Table Of Content,
JournalofResearch ontheLepidoptera 37: 37-45, 1998 (2003)
Seasonal fluctuation and mortality schedule for
immatures of Hypna clytemnestra (Buder),
uncommon
an neotropical butterfly
(Nymphalidae: Charaxinae)
Arlindo Gomes-Filho
Curso de Pos-Graduagao em Ecologia, IB, C.P. 6109 Universidade Estadual de Campinas
13083-970 Campinas, SP, Brazil
E-mail: [email protected]
Abstract. I describe the pattern ofabundance and a mortality schedule for a
populationofHypnaclytemnestrahuebneri (Butler) (Nymphalidae: Charaxinae)
an uncommon neotropical butterfly inhabiting southeastern Brazil. Over a
one year period I gathered data on the abundance of immatures through
periodic censuses on 65 host plants, whereas adults were trapped monthly. A
marked seasonal variation in abundance of immatures was detected, with a
peak during the wet season. Adults were present throughout the year, but at
very low numbers. The construction of a life-table showed that the main
mortalityfactors acting upon immatureswere parasitoids and predators. Eggs
and medium to large-sized larvae suffered higher mortality, characterizing a
mixedType II/IIIsurvivorshipcuiwe. Thedata highlight theeffectofpredators
upon larval stage as well as the great impact of parasitoids on eggs, which
contrasts to the usually low intensity ofegg parasitism reported for temperate
species. These results reinforce general trends detected in recent literature
reviews for more abundant and/or pest species towards the importance of
natural enemies as mortality factors ofherbivorous insects.
Key words: Hypna, life-table, parasitism, predation, seasonality, survivorship
curve.
Introduction available, encompassing several different groups.
TheorderLepidopteraisrelativelywell represented,
To achieve a fuller understanding of the although manystudies refer to veiy abundant and/
processes and factors governing fluctuations of orpestspecies (reviewsin Dempster 1983; Courtney
animal populations, an important first step consists 1986; Cornell & Hawkins 1995; Hawkins et al. 1997;
of describing these fluctuations in the field at Cornell et al. 1998). Yet, for neotropical region,
differenttime-scales,includingspecieswithdifferent despite the increasing number of studies on
life-histories inhabiting different habitats and popidation dynamics of adult butterflies (e.g.
showing different patterns of abundance. The Ehrlich & Gilbert 1973; Vasconcellos-Neto 1980;
increase in the number of descriptive studies in Saalfeld&Aiaujo 1981; Quintero 1988;Freitas 1993,
different ecological contexts may lead to the 1996; Ramos & Freitas 1999, Vanini et al. 2000;
detectionofhiddenpatterns (Price, 1991) andmake Freitas & Ramos 2001, Freitas et al. 2001), field
possible the establishment ofmore comprehensive investigations on immature populations of
andreliablegeneralizations (e.g. Cornell &Hawkins Lepidopterain natural habitatsare still scarce. This
1995; Hawkins et al. 1997; Cornell et al. 1998). is especially true for investigations employing life-
For temperate regions many of studies on table methods, ofwhich the few examples include
demography of herbivorous insects are already thestudiesofCosta (1991) on thebutterflyHypothyris
38 J. Res. Lepid
nmonia daetn (Bclv.) and Caldas (1995a,b, 1996), the trails or on the borders of the forest. Leaves
dealing with the popnlational dynamics of' the vary in size (10 to 20 cm) depending on the height
juvenile stages of Anaea ryphea (Cramer) in ofplants. During the dry season plants tend to dry
southeastern Brazil and in Panama. This paucityof out,withareductionin theproductionofnewleaves
data on mortality schedules for immature stages of and in their nutritional quality (unpublished data).
neotropical Lepidoptera inhabiting natural systems Younger larvae (first to third instars) construct
is even more striking for uncommon species. frass-chains (pers. obs.) which are used during the
In a population study of the butterfly Pieris whole larval period. Larvae are sedentary, staying
virginiensis Edw’mxh, Cappuccino & Kareiva (1985) on the frass chains most of the time, leaving these
correctly argued that because in natural habitats sites only to feed during short bouts. Fifth instar
most insect species are rare, the understanding of larvae leave the host plants to pupate. Adults
the relationships between these species and their sometimesflyalongstinnytrailsandforestgaps, but
host plants is essential to any theoiw ofplant-insect during mid-day males usually perch on sunny sites
interaction. Besides that, the greater emphasis put along trails, displaying territorial behavior. Like
in studies of very abundant or of economic value otherCharaxinae, theyfeedon rotten fruits,carrion
species coidd lead us to biased generalizations and feces (Young 1982; De’Vries 1987).
(Hayes 1984; Hawkins et al. 1997). In a review on
novel approachestostudiesofpopulation dynamics, Studysite
(iappticcino (1995) called for more studies of rare Thestudywascarriedoutatthe Reservade Santa
species, in spite of the obvious difficulties of data Genebra, located at Campinas (22° 44’ S, 47° 06’
gathering in these cases due to the low population W, elevation 670 m), state ofSao Paulo, Brazil. The
sizes. If we want to get a broader and unbiased reserve is a 251,7 ha patch ofdisturbed subtropical
pictureofmortalitypatternsforherbivorousinsects, semideciduous moist forest, surrounded by crops
it is clear that more quantitative descriptive studies of corn and soybeans, and other human
are needed. infrastructures. Mean monthly temperature varies
In this study I describe the seasonal abundance from 18°Cto29°C,with dailyfluctuationsofasmuch
fluctuation and mortality schedule for immature as20°CfromJulytoSeptember (Morellato &Leitao-
stages (eggs and larvae) of a population of the Filho 1995). There is a dry season from April to
butterfly Hyfnui clytemnestra huehneri (Butler), a Augtist, characterized by low temperatures and low
widelydistributed but locallyuncommon charaxine precipitation, followed byawarmerandwetseason,
(Nymphalidae) inhabiting southeastern Brazil. from September to May (Fig. 1).
Material and methods
Study organisms
Hypna clytemnestra (Butler 1866) is a medium-
sized (forewinglength 40-45 mm), relativelycryptic
butterfly. A general description of the species can
be found in Comstock (1961). In the study area
females layeggs singlyon the underside ofleaves of
Croton florihundus Sysreng (Euphorbiaceae) a
,
latescent pioneering plant commonly found in the
reserve. This species is also used as host plant by
another Charaxinae butterfly, Anaea ryphea, which
is veiy abundant in the area (Caldas 1994, 1995a)
and occasionally by A. appias (Hiibner), A. otrere
(Hiibner) and possibly A. arginussa (Geyer). Friegg.i1o.nCldiumratiincgditahgerasmtuofdythepeRreisoedrva(NdoevSeamnbtearGlen9e9b8ra-
Individuals of C. flordmndus of varying sizes, from December1999). Hatched = humid period, black =
seedlingstosaplingsortreesarefoundinbothsunny superhumid period and dotted = dry period (following
Walter, 1985).
andshadyareas, isolatedorin patches, mostlyalong
37: 37-45, 1998 (2003) 39
Mortality pattern of Hypna clytemnestra population To evaluate the variation in adult abundance of
To investigate the abundance and mortality H. clytemnestra} employed 12 traps (p. 35 in DeVries
pattern of H. clytemnestra immatures, from 1987) baited with fermented bananas, distributed
November 1998 to November 1999 I inspected 65 as follows: four traps on the forest edges, four traps
previously tagged plants of a population of C. along the central trail (study trail), and four traps
Jloribundusforthepresenceofeggsandlarvae. They inside the forest. Forest edges were characterized
were inspected at three-day intervals from early to by an abrupt transition between forest and open
mid-season, and once aweakfrom Februaryon. All fields with crop vegetation. Traps on the central
tagged plants were distributed along the edges ofa trail were in the middle ofthe forest, but in a kind
m
1,160 central trailwhich passes through the area. of habitat looking like a gap, due to the relatively
I individualized eggs and larvae through a open canopy and more intense light penetration,
combination ofIndiainkmarkingson leaflimband whereastrapsinside theforestwere inamore humid
plastic rings placed around leaf petiole. These and shady environment. Traps were hung 1.5 to
procedures permitted recordings of immature 3.5 m above the grotmd. Each sampling consisted
numbers and positions on each leaf and on each ofopeningtrapsaround noon and closingthem the
individual plant, making it possible to track their followingdayatthesame time. Capturedbutterflies
development and survivorship (cf. Caldas 1995a). were individually marked on the hindwing with a
Eggs and larvae that disappeared between two felt-tipped pen and then released. I took four
consecutive inspections were assumed as have been samples each month, from March 1999 to Februai^
preyed upon. 2000, totaling 48 samplings.
I constructed a multiple decrement life-table
(Carey 1993), which permits identification of the
stages oflife suffering the highest mortality as well Results
as evaluation of the effect of different mortality
factorsactingsimultaneously. I carriedoutacompe- The population of H. clytemnestra showed a
ting risk analysis (Carey 1993), a mathematical seasonal pattern of abundance lluctnation for the
approximation that permits inference ofthe effect immaturestages notseen in theadults (Fig. 2). The
ofone cause of mortality when another cause that number of eggs and larvae increased from a very
occurssimultaneouslyiseliminated. In thismethod, low level in late November/early December 1998
ifwe have two causes ofmortality, Aand B, is the to a peak in lateJanuai'y/eaiiy March. This peak
proportion ofindividualsinferred todiewhen cause was then followedbyasudden reduction in number
B is absent, and is the proportion ofindividuals of immatures to reach the level observed at the
inferred todieifcauseAisabsent. D and denote beginning of the growing season. During the rest
^
the fraction ofall individuals observed to die from
cause A and B, respectively. Then q^ can be found
by solving the equation;
aq^^ + bq^ + c = 0
where
a= + = - (D^ + D^)
^ = De(D,+ D3) qB = qP^/D,
Months
For a detailed explanation and rationale of the
method see Carey (1993: 26-29). Fig.2. Abundancefluctuation of immaturesandadults
ofHypnadytemnestra^XtheReservedeSantaGenebra,
Campinas,SRfrom November/1998toFebruary/2000.
40 /. Res. Lepid.
oftheyearjustafewimmatures (less than 5) oreven Eggs of H. clytemnestra were parasitized by an
none (in the dryseason) were recorded on the host Eulophidae species. Mortality of first and second
plant population. instars were less intense (7.0 and 22.5%,
The number of adults trapped monthly was respectively) than those ofthird and fourth instars
consistently low (0 to 6), resulting in a total ofonly (54.8 and 64.3%). Only 2.3% of the eggs reached
28 individuals captured (as a comparison, at the fifth instar. Mortalityofthe fifth instar larvae could
sameperiod419 individualsoftheabundantspecies not be estimated since larvae in this phase of
A. ryphea were trapped). No clear peak in adult development leave the plants to pupate. All larval
abundance was detected (Fig. 2). The captured mortality was attributed to predation. Even if we
individuals were not uniformly distributed among assume mortality factors acting upon fifth instar
habitats (X- = 8.85; df = 2; p = 0.012). Most were laiwaeandpupae tobe negligible (which isunlikely)
capturedon the central trail (50.0%) and inside the the percentage of immatures actually reaching
forest (42.9%),whilefewwere trapped on theforest adulthood is less than 2.3%.
edge (7.1%). Onlyfourindividualswere recaptured, Thus,eggsand medium tolarge-sizedlaiwaewere
with the following recorded residence times (i.e., the stages with greatest risk of mortality (Table 1).
time elapsed between capture and last recapture): Even correcting for differences in stage/instar
3, 18, 23and 36days. Itshouldbe noted that despite duration by considering probability ofsurvival on a
the extremely low abundance, adults were trapped daily basis, this pattern ofmortality did not change,
even during the dry season months. indicating that the tendency for more intense
In all, 211 immatures were followed from egg to mortalityofeggsand largerlanaewasnotanartifact
death. The eggstage suffered highest mortality (ca. due to differences in amount of time exposed to
80.0%),attributed toboth parasitismand predation naturalenemies (seevaluesinside parenthesisin the
(Table 1, Fig. 3). Despite this intense mortality, 1 first column ofTable 1). Therefore the intensity of
did not directlyobserve predation on eggs or larvae mortality suffered by eggs and all larval instars
of any instar during censitses, though on two considering the whole season generates a mixed
occasions I observed eggs being parasitized. survivorshipcurveofTypesII/III, basedon Deevey's
Although these eggs are very small, they can be (1947) general classification (Fig. 3).
readly seen with the naked eye after one gets used The competingriskanalysisforeggsshowed that
to the contrast between leafsurface and egg color. ifpredation was eliminated as a cause ofmortality,
Several events ofegg parasitism were also observed egg parasitism alone would kill 58.1% of the eggs,
foreggsofthebutterllyA. rypheaon thesame plants. instead of the 42.6% actually killed. If parasitism
Table 1. Themultipledecrementlife-tableforimmaturestagesofapopulationofthebutterflyHypnaclytemnestras\.uA\e6during
1998/1999attheReservedeSantaGenebra, Campinas, SR Brazil.
Stage ^ Number Fraction Probability Fraction of Fraction of deaths Daily
beginning living at of death all deaths from
probability stage the beginning
of survival 2
of interval predation parasitism
Kx alx aqx adx.^ adxl adx2 Px
Egg (5) 211 1.0000 0.7962 0.7962 0.3697 0.4265 0.7275
Instar (4) 43 0.2040 0.0698 0.0142 0.0142 0.0000 0.9820
1
Instar II (7) 40 0.1900 0.2250 0.0427 0.0427 0.0000 0.9642
Instar III (6) 31 0.1470 0.5484 0.0806 0.0806 0.0000 0.8759
Instar IV (6) 14 0.0660 0.6429 0.0427 0.0427 0.0000 0.8423
Instar V (6) _S 0.0230 - - - - -
^-ValuesInsideparenthesisrefertothemean numberofdays(tjspentineachstagebasedonfielddata
DailyptobabilityofsutvivalobtainedasPx=(1 -qj
37: 37-45, 1998 (2003) 41
100 -1
80 -
Predation + Parasitism Predation
Parasitism alone alone
Fig3. Survivorshipcurveforimmaturesofapopulation Predation + Parasitism Predation
ofHypnaclytemnestras\u6\e6foroneyearattheReserve Parasitism alone alone
de Santa Genebra, Campinas, SR Dashed line
representsatheoreticalsurvivorshipcurvewithconstant Fig.4. Intensityofimmaturemortalityinferredfromthe
rateofmortality(Type 11). competing riskanalysisappliedforeggsalone(A)and
foreggsandlarvalinstarscombined(B). Leftbarshows
theoriginallife-tableresults,middlebarshowstheimpact
ofparasitism ifpredatorswerenotactingand rightbar
shows the impact of predation in the absence of
was eliminated, 49.0% ofthe eggs would have died parasitism.
from predation as compared to the 36.9% (Fig. 4).
Wdien mortalitywasconsideredduringbotheggand
all larval instars, elimination of predation would
increase parasitism from 42.6% to 71.7%, whereas On the other hand, the proximity of the dry
if predators were acting alone they would be season leads to host plant deterioration (i.e.
responsible for as much as 91.7% of all deaths, a accumulated leaf damage, reduction in water and
significant increase over 40.0% (Fig. 4). nitrogen content),which maysometimes result in a
reduction in reproductive activity in seasonal
habitats (Jones 8c Rienks 1987; Braby 1995). In
Discussion addition to that, the increase in immature density
in the middle ofseason mayincrease the encounter
Hypna dytemnestra immatures showed a marked and attack rates on eggs and larvae by parasitoids
seasonal fluctuation in abundance during the year, and predators, which will probably buffer the
a pattern not followed by the adult stage. The population increase. The rate of parasitism for
increaseinimmaturenumberwaswellsynchronized fotirth instarlarvae ofA. rypheafeedingon thesame
with the increase in rainfall in the wet season. hostplantseemed toincreasein responsetoincrease
During this time there is an increase in food in larval density (Caldas 1996). Other examples of
availability, since a greater number of new leaves, positive density dependence action of parasitoids
of better nutritional quality are produced by host and predators on herbivorous insects can be found
plants (unpublished data). A likely scenario is that in Stiling (1987, 1988).
the arrival of summer also results in hotter and In addition to the positive effect mediated by
longer days and larvae from eggs hatching at this improved host plant quality, a possible negative
time will develop in a warmer environment and effect of heaw rainfall on immatures of Hypna is
might be feeding on more abundant and better the mortality ofeggs and larvae by dislodging from
qualityleaves. Thesesimultaneouschangesin adult leaves (e.g. Blau 1980; Courtney & Duggan 1983).
and larval environment will act in combination, Althoughsuch effectwasreportedbyCaldas (1995a)
favoring a faster larval development, shortening for larvae of the butterfly A. ryphea using the same
generation time and leading to a rapid increase in host plant in the area, itwas not observed for larvae
the butterfly population. of Hypna.
42 J. Res. Lepid.
Young (1981) evaluated theseasonal distribution more abundant pierids, with less intense mortality
of two species ofCharaxinae in a dryforestofCosta during the egg stage and final instars and a higher
Rica, Anaea morvus Boisduvali and Anaea {Zaretis) survival ofthe initial instars (Courtney 1986). Some
ity.sCramer. Forboth species, immaturesandadults other studies showing similar results are those of
were abundant mainlyin the wetseason, being rare Courtney (1981) and Hayes (1981) - Pieridae, and
or even absent during dry season. He detected a Blau (1980) and Rausher (1980) - Papilionidae,
low level oflarval parasitism and suggested that the while Watanabe (1981) and Feeny et al. (1985)
seasonal patternofabundanceofAnampopulations found more constant rates of mortality from eggs
was a response to a reduction in food quantity and to late instars for species ofPapilio, characterizinga
quality. A marked seasonality in immature Type II survivorship curve.
abundance was also reported for the butterfly H. The competing risk analyses for Hypna revealed
ninonia daeta, which reached high densities at the thatfortheeggstageboth predationandparasitism
end ofthe wet season in a forest patch in southern are equally important as mortalityfactors, since the
Brazil (Costa 1991). Host plant abundance and elimination of each one of them leads to a similar
quality was suggested as of primary importance in compensation (increase) in theintensityofmortality
the dynamics of H. Jiinonia daeta. The correlation caused by the other. When both eggs and larvae
between fluctuation of insect abundance and areconsidered, predatorsseem tobeplayingamore
seasonalityofrainfallandfoodavailabilityin tropical important role, since predation would compensate
habitats has been reported previously by Wolda better for the absence ofparasitism than vice-versa.
(1978a, b), but despite the good match between In most published studies mortality was caused
rainfall and population fluctuation, it may be that by different factors at different stages/instars (see
rainfall pattern is not the main factor causing the review in Dempster 1984). Eggs can fail to hatch
increase in immature population ofinsects (Wolda due to apparent infertility, suffer from disease and
1988). bacterial attack, be dislodged by rain, die from
The general mortality pattern described here dissecation or other unknown physiological causes,
consists of higher mortality of eggs and late laiwal beparasitizedorpredated (Baker 1970;Parker 1970;
instars and high survival ofsmall larvae. However, Young & Moffet 1979; Hayes 1981; Watanabe 1981;
in a population ofA. npheastudied in the same site Courtney & Duggan 1983; Caldas 1995a, 1996).
andfeedingon thesamehost plant, firstinstarlanae Small larvaecanbedislodgedbyrain,fail toestablish
was the stage showing higher mortality during the in the host plant due to physical or chemical
season,whichwasattributedmostlytopredationand barriers, be parasitized or predated by small
to intense rain (Caldas 1995a, 1996). Nevertheless, arthropods (Baker 1970; Blau 1980; Courtney 1981;
in these previous studies mortality of eggs was not Hayes 1981; Watanabe 1981; Courtney & Duggan
quantified. On theotherhand, the mortalitypattern 1983; Caldas 1995a; Ohsaki & Sato 1994, 1999),
reported for immatures ofH. ninoniawas similar to while larger larvae tend to be predated by
that found for H. clytemnestm, with more intense vertebrates, especially birds (e.g. Pollard 1979;
mortality suffered by eggs and final instars (Costa Watanabe 1981).
1991). In this studythe onlycause ofmortalitydetected
In temperate regions, population studies directly was parasitism of eggs. Parasitized eggs
including the construction of life tables for change colourinto metalicgray. Predationcanonly
immature stages were carried out for some pierid be inferredbythedisappearance ofeggsandlarvae.
species (e.g. Courtney& Duggan 1983; Cappuccino Despite no observation of a predation event upon
& Kareiva 1985; review in Courtney 1986). A Hypna immatures, possible invertebrate predators
different mortality pattern was reported for ofeggs and small larvae in the area would be ants,
Anthochariscardamines (L.) in Britain,witharelatively spiders and wasps, the first two groups being
low egg mortality and low survival oflarvae in early relatively abundant on C. floribundus. Evidence
instars (Courtney & Duggan 1983). The extremely supporting this are observations of ants preying
lowegg parasitism isopposed to the high parasitism upon eggs (J. M. Queiroz, pers. com.) and of a
rate found for Hypna. For the rare Pieyis virginiensis jumping spider (Salticidae) preying upon a second
larval survivalwassimilarto those reportedforother instar larvae of A. ryphea. The direct observations
37: 37-45, 1998 (2003) 43
of predation on immatiires of A. ryphea were inability ofadults to cross open fields and colonize
probablyfavoredbyitshigherabundance,andthere new adequate habitats all acted to shape the
is no reason to believe that these same predators populationsatlowdensities (Cappuccino &Kareiva
would notkillimmaturesofHypnaaswell. Potential 1985). Except for unfavorable climatic conditions,
predators oflarge larvae are wasps and birds. most of the cited factors do not apply to H.
Attacks by predators, parasitoids and pathogens clytemnestra. Its low abundance, even during the
were the most frequently cited sources ofmortality middle of the wet season when individuals are
(48%) for immatures ofherbivorous insects in 530 supposed to have been the best environmental
published life-tables evaluated by Cornell and conditions,seemstobeshaped mainlybytheintense
Hawkins (1995), which included some studies on mortalitysufferedbythe immaturestagesdue to the
Lepidoptera. In a more quantitative analysis of83 action of natural enemies, namely high parasitism
life tables for 78 herbivorous insect species, and predation upon eggs and predation upon
predators appeared as the dominant natural enemy larvae.
(ascomparedtoparasitoidsandpathogens) ofpost-
egg stages in the tropics and subtropics, whereas Acknowledgements
parasitoids are dominant in temperate zone
(Hawkins et al. 1997). For the population of H. I am grateful to the Funda^ao Jose Pedro de
clytemnestra investigated, inhabiting a tropical and Oliveira for the permit to work in the Reserva de
seasonal environment, natural enemies emerged as Santa Genebra and to the direction of CEPAGRI/
the main mortality factors. Considering all stages Unicamp for making the meteorological data
and instars, predators played amajor role, agreeing available. Andre V. L. Ereitas, Eelipe A. P. L. Gosta,
with the pattern suggested for the tropics in the Elavia de Sa and Jarbas M. Queiroz made helpful
above review. For the egg stage, death rate was comments on previous versions of the manuscript.
equally due to parasitoids and predators, but the I thank two anonymous reviewersforimproving the
formerkilledahigherfraction ofeggsofHypnathan manuscriptfurther. The authorwas supported bya
is usual in species oftemperate regions. Graduate fellowship conceived by the Gonselho
Regarding habitat use, adults of Hypna seem to Nacional para o Desenvolvimento Tecnologico e
use equally well both shady, inside forest and gap- GientiTico (GNPq).
like habitats, avoiding to some degree more open
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