THE UTILIZATION OF SPECIES LARVAE PLEXIPPUSdownloads.hindawi.com/journals/psyche/1973/028693.pdf ·...

THE UTILIZATION OF VARIOUS ASCLEPIAS SPECIESBY LARVAE OF THE MONARCH BUTTERFLY,

DANAUS PLEXIPPUS

BY JAMES M. ERICKSON*Dept. o Entomology, Cornell University

Ithaca, New York, 485o

INTRODUCTION

Plants of the genus Asclepias are well known to. contain highconcentrations o cardiac glycosides (cardenolides). It is generallysurmised that such cardiac stimulants unctio,n to, protect plantscontaining th,em against insect and vertebrate herbivores (Euw et al.967). In addition, some insects w,hich are adapted to. eed onAsclepias plants store cardiac glyco,sides apparently as a means o.protection against vertebrate predat.ors which ind he compoundsdistasteful (Brower and Brower 964, Brower 969). It was bymeans of such an herbivore-predato,r interaction, bluejays eedingon monarch butterflies, Danaus plexippus L. (Brower 969, Broweret al. 968), that a spectrum o.f palatability was detected amongmonarch butterflies reared on various species ,o milkw.eed. It issurmised that this spectrum of toxicity to a vertebrate predator reflectsa spectrum of concentrations o cardiac glycosides in the differentspecies o the insects’ larval ood plants (Brower and Brower 964,Brower et al. 967, Brower 1969). However, quantitative andqualitative data ,or cardenolides in Asclepias leaves, are at best in-complete (Reynard and Morton 942, Kupchan et al. 964, Duffey97o, Singh and Rastogi 97o, Feir and Suen 97, Duffey andScudder 972, Scudder and Duffey 972, and Eggermann andBongers 972).The following experiments were undertaken to determine

whether a dierential response by D. plexippus larvae to their hostplants could be detected by measuring their efficiency o ood utiliza-tion and whether such a response would support the concept o aspectrum o toxicity. It seemed conceivable that detoxication orstorage o cardiac glycosides might require expenditure o. energyand could be detected by a lowered eeding efficiency. In addition,Brower et al. (I972) have speculated that there is a reduction in

*Present address: Dept. of Biological Sciences, California State Univer-sity, Hayward, California 94542.Manuscript received by the editor June 18, 1973.

230

973] Ericbson Danaus plexippus 3

general viability of monarch adults which have stored higher con-centrations of cardiac glycosides. To test this hypothesis the fertilityand fecundity of adult monarchs was determined.

METHODS AND MATERIALS

Groups of intact larvae of D. plexippus were taken from thesecond generation of a culture o.unded t:rom wild insects taken nearIthaca, New York, and were reared in the laboratory on one o.f thefollowing species of Asclepias host plants: A. curassavica, A. syriaca,A. incarnata, or A. tub,erosa. Newly molted 4th-instar larvae wereplaced individually in glass petri dishes (Pyrex, Ioomm )< 15rnm)lined on the bottom with a piece of Whatman No. filter paper.Mature and uninjured leaves of the native species were gathered inthe field each day from plants growing in open sunlit areas, andleaves of A. curassavica were collected from plants grown in thegreenhouse. All leaves were sealed in plastic bags and used within2 hours. These randomly collected leaves were split along the mid-rib, one half weighed and offered to the larv.ae and the other halfused to determine the percent dry matter in the. leaf material(Waldbauer I96o, I964). Leaves were replaced and feces collectedevery 24 hours.

All the larvae were placed in a controlled temperature room,except for the period of time each day during which new food wasoffered to the larvae and the feces collected. The. room vas keptrelatively co.nstant with day-night temperatures of 22 and 18,respectively, and with a relative humidity of approximately 55%.The photoperiod was regulated at a 16-8 hour light-dark cycle.The dry weight of food ingested was estimated following the

techniques of Waldbauer (I96O, 1964), except that plant materialwas lyophilized instead of oven-dried. The dry weight of the foodutilized or assimilated was assumed to be the dry weight of the foodingested minus the dry weight of feces. An additional group oflarvae was reared along with the experimental larvae, and thesewere s.acrificed to determine the dry weights, and thus, the per-centage dry matter of the larvae. Indices of foo.d utilizatio.n weredetermined following the methods of Watdbauer (196o, 1964,I968). Many terms have been used both by ecologists and byphysiologists to describe various measures and indices of food

1Specimens of the insects used in this research have been deposited in theCornell University Insect Collection, Lot 1023, Sublot 14. Specimens of theplants have been deposited in the Bailey Hortorium, Cornell University.

232 Psyche [September

utilization and efficiency. Relationships between many of these termsare discussed by Kozlovsky (I968) and Waldbau,er (I968).As an index of digestibility the ratio of the amount of food

assimilated to the amount of food ingested, referred to as the’Assimilation Efficiency’ (Odum, 971 or the ’Coefficient of Di-gestibility’ (Waldbauer 964, I968, House I965), was used. Inpractice, this measure is only an approximation .since the numerator(as determined by the standard gravimetric technique) does notquite represent the amount of food .actually assimilated (Wa’tdbauerI968). This slight error is due to the presence of metabolic wastesin the feces in addition to the undigested ood (Lafon I95I), butHiratsuka (I92O.) and Waldbauer I964, I968) point out that thisdifference between true and measured assimilation efIiciencies isnegligible.The efficiency with which ingested food is converted to biomass

is calculated by dividing the dry weight of food ingested into thedry weight gained by the larva. This ind’ex, referred to by physiolo-gists as the ’Efficiency of Conversion of Ingested Matter’ (Wald-bauer 968) and by ecologists as the ’Ecological Growth Efficienc.y’(Odum 97I), is an overall measure of an animal’s ability to utilizefor growth the food ingested.The efficiency with which digested food is converted to biomass is

calculated by dividing the dry weight of food assimilated into t’hedry weight gained by the larva. "Ihis index, referred to by Wald-bauer (I968) as the ’Efficiency of Conversion of Digested Matter’and by Odum (97I) as the ’Tissue Growth Efficiency’, decreasesas the proportion of digested food metabolized for energy .and main-tenance of physiological functions increases (Waldbauer I968).The relative growth rate is calculated by dividing the mean dry

weight of the larva times the duration .of the instar in days into thedry weight gained by the larva during the stadium (Waldbauer968). This index reflects the rate at which biomass is added by alarva corrected for any size differential betw.een groups of larvae.The ’Respiratory CoefIicient’ (Lindeman 942) is described as

the ratio of respiratory and maintenance loss. to the net secondaryproduction or biomass increase. This coefficient is calculated bydividing the total calories lost through respiration and maintenanceby the total calories added to the insects’ biomass. This ratio iswhat may be termed an ’Energy Production Cost Ratio’; the smallerthe .coefficient or ratio, the more eNcient the larva is at allocatingenergy to biomass, the larger the coefficient, the. greater t,he number

1973 Erickson Danaus lexiIlus 233

ot: calories lost through respiration and maintenance per caloriealk)cated to biomass.Of general interest to ecologists is the ’Principle o. Allocation’

described by Cody (1966). Organisms have a limited amount ofenergy to spend and will be selected to partition this energy in diE-erent ways depending upon changing physiological or environmentalconditions. Any activity of an organism, or more precisely, theenergy expenditure for that activity, can be. viewed only in relationto all other demands for energy. To descry any increased ’cost’ ofdetoxii:ying or incorporating cardenolides by D. plexippus larvaewhen reaved on Asclepias host plants with known toxicity spectrum,a larval energy budget based on dry weights was constructed. Calo-rific values oi: the larval oo.d plants, feces ,and larvae were deter-mined by means o1: a Phillipson non-adiabatic microbomb calorimeter(Gentry and Wiegert Inst. Inc., Aiken, C.S.) (Phillipson I964).The lyophilized plant material was. subjected to ve replicationswhereas lyophilized larvae .and feces were subjected to three replica-tions for the determinatio.n o cal,oriqc values.The nitrogen content of the le.a material was determined by the

Kjeldahl method for total nitrogen (Williams I964). A minimumof three replicate samples were obtained for ea.ch o the plant species.

For the purposes of ood utilization and et:ficiency determinations,the experiment was concluded when the larvae moited into theultimate instar. The larvae were then reared through to. the adultstage on the same experimental plants that they fed upon in theutilization experiments. All adult emales were hand paired andplaced individually in a meter square screen cage with one A.curassavica and one A. syriac,a plant of approximately the same ,ageand condition. Records were kept each day o the number of .eggslayed per emale and the percentage of these eggs which were fertile.The data ,are generally presented as a mean and standard error

for the larvae in any particular treatment group. The variousexperimental parameters and indices were subjected to one-wayanalysis of variance to determine differences in efficiencies or develop-mental rates anaong the various larval oo.d plants.

RESULTS

Various plant parameters differed greatly among the four Asclepiasspecies offered to the monarch larvae (Table I). The leaves ofA. tuberosa were significantly higher in dry matter content than theother three species. No significant difference in caloric content could


v,,,. % %

1973 Erickson Danaus #lexip[us 235

be found among the ]our dsclepia’s species. The nitrogen contentof the leaf ma.terial did not vary significantly for A. curassavica,A. syriaca, and d. incarnata but the leaves o,f A. tuberosa co,ntaineda little more than one half the total nitrogen content of the otherplants examined.The proportion .of ingested foo,,d which was digested and ,as-

similat,ed (’assimilation efficiency’) averaged about 5o% for allexperimental host plants, except for d. syriaca which was signifi-cantly higher (P(o.os) with a mean of approximately 58%(Table 2). The efficiency with which ingested matter was con-verted to biomass ranged ro,m 29.59% for larvae reaved on d.syriaca to 6.39% fo.r larvae reared on d. tuberosa (P<o.oI),whereas the efficiency of co.nversion of digested matter ranged from53.3o% for larvae reared on d. curassavica to 34.0’4% for larvaereared on d. tube’rosa (P(o.o). The duratio,n of the 4th stadiumalso varied significantly (P(o.oI) with larvae o,n d. curassavicahaving the shortest duration (2.5 days,) and larvae on d. syriacahaving the longest duration (2.55 days). The amount of biomassgained per day per lavva also varied significantly (P(o.os) withlarvae reared on d. curassavica gaining the most weight (6.4zmg/day) and larvae on d. incarnata the least (2.7o nag/day).,’Of great interest, however, is that the relative growth rate did notvary ,significantly for the larvae feeding o,n the four dscle/ias species,

The total allocation of energy by the larvae on the differenthost plants can be found in Table 3. The tarvae reared on A.tubeosa ingested and assimilated almost twice as many calories as,

larvae reared on d. curassavica or d. syriaca. The total nlamber otcalories allocated to larv,al biomass did not vary to, any extent amongthe AscleDias species; ingestion of more calo,ries by la,rvae reared onA. incarnata and d. tuberosa was balanced b.y greater costs for res-piration .and maintenance. The ratio of the total number o,f calories.allocated to an increase in larval biomass to t,he total caloriesassimilated ranged trom approximately 65% by larvae, reared onA. curassavica to approximately 32% for larvae reared on d. tuber-osa. The respiratory coefficient also ranged from o.53 (d. cur,as-.savica) to 2.I6 (d.,tubenosa).

There was no difference in the mean length of the larval stage, orthe pupal stage among larvae reared on the various Ascle/ias species(Table 4). Larval survival was IOO% on all host plants exceptA. incarnata where 9o% of the larvae survived to the adult stage,Fecundity and fertility does not vary significantly; the mean numberof eggs layed per female ranged from IO3.7 for females reared on

Psyche

+! +1 +1 +1 +1 +1

m +! +1 +1 +1 +1 +1

+1 +1 /! +1 +I +1

+1 +! +1 +I +1

September

1973 Erickson Danaus #lexi##us 237

.4. curassavica to I7.2 .or females reared on d. syriaca. The meanper cent o eggs hatching ranged rom 87.3% (.4. incarnata) to

93.2% (.4. tuberosa).

DISCUSSION

One o. the major concerns o modern ecology is the descriptionand explanation o the energetic relationships between and withinvarious communities. A knowledge of the f.ood utilization efficiencyof insects is thus of particular importance to ecology .since insectsexert a substantial influence and impact on almost all terrestrial orresh water communities. The ecological significance of such energyuti]ization studies have been extensively revievced (Englemann 955,Phillipson 955, and others).

It seems apparent that adaptive nutritional di6erences in hostplants must be sought on a quantitative lev,el and that meaningfulcomparisons of food utilization and nutrition will not emerge untilquantitative studies are carried out. The determination of absoluterequirements or dietary constituents dep,ends upon the measurementof ood or nutrient intake. Dierences in tood eciency can bedemonstrated only be measuring intake and growth. B/Ieasur,ementoi: the i:o.od intake and the utilization o this ood elucidates to. agreat degree the physiological processes occurring in an insect sincepatterns of utilization may be dierent although ood sources aresimilar in their ability to support growth. For instance, low oodintake may be offset by a high utilization o,f ingested or digested foodand a very high food intake may well lead to a very low efficiencyin the utilization of ingested or digested matter.

In this experiment, the assimilation efficiency of the larvae did notvary significantly among the various Asclepias host plants except forlarvae reared on A. sriaca which had an efficiency about 8% higherthan larvae on the other host plants. This means that the larvaereared on the various host plants were digesting and excreting ap-proximately equal amounts of food. The efficiency with whichingested food and digested food are utilized varied significantly withlarvae reared on A. curassavica and A. sriaca having the highesteciencies and iarvae reared on A. tuberosa the lowest (Table 2).The efficiency with which digested ood is utilized for growth willvary not only with the maintenance ,and respiration requirements forenergy but also with the balance of nutrients in the ood source.Larvae reared on A. tuberosa ingested almost twice as much foodduring the 4th instar as larvae reared o,n the other three host plants

Psyche [September

973 Erickson Danaus plexippus 239

(see Table 3). As the ingestion rate increases, there is a negativecorrelation with the efficiency with which ingested or digested matterare utilized (Waldbauer 968). This reduction in overall gross andnet efficiency has been shown for Prodenia larvae (Soo Hoo andFraenkel 966) and by House (r965). The larvae reared on A.tuberosa may be viewed as being extremely ’wasteful’ o.f the potentialcaloric content of their ood, most likely passing great quantities ofood through the digestive tract to secure a supply 6f some limitingnutrient or substance. The leaf material does not vary to any sig-nificant degree among the dsclepias species tes’ted in terms of caloriccontent (Tabl,e ), whereas the leaves of A. tube’rosa contain a littlemore than one half the nitrogen content of the )ther three species.

It has been suggested that the water content of o.od material wiltgreatly affect the utilization of this material. It is generally the casewith the swall.owtail butterfly, Papilio polyxenes, that the efficiencyof utilization of ood decreases as the dry matter cntent of t’he foo.dplant increases (Erickson and Feeny, in preparation). In this ex-periment, there is a significant difference in the dry matter contentof the leaves, with A. tuberosa having the highest dry matter con-tent at approximately 2% and A. incarnata and A. syriaca thelowest dry matter content at about I7% (Table ). It has beenshown in this laboratory, that by varying the water content of leafmateriai, the utilization of ood by the cecropia moth, I-Iyalophoracecropia is greatly affected (J. M. Scriber, in preparation)., Theeffect is shown not in a,n increased intake rate, as occurs in monarchlarva.e, but in lengthened larval development times, in which thetotal food intake is increased but the rate of this intake, remainsrelatively constant. It thus appears that the dry matter content ofAsclepias leaves may have some influence on the utilization efficienciesbut not to the degree found in this experiment.

In keeping with Cody’,s (966) ’Principle of Allocation’, I at-tempted to descry any increased ’cost’ for D. plexippus larvae to

detoxii:y or to incorporate cardeno.lides.. It is well known that A.curassavica is highly toxic and contains at least 5 cardenolidies(Kupchan et al. 964, Duffey 97o), three of which have beenisolated from distasteful D. plexippus larvae (Parsons 965, Reich-stein 967) incorporated there as a defense against vertebrate preda-tors (Brower .and Brower 964, Br.ower et al. 967, Brower 969).Asclepias syriaca has been found to be only slightly toxic to verte-brates and to contain at least seven cardiac glycosides (Reynard andMorton 942, Duffey 97o, and others). Asclepias incarnata andA. tuberosa are known to. contain cardeno.lides but in much lower


TABLE 4. Length of pupation, fecundity and fertility of monarch butterfliesraised on vario.us plants of the genus ‘4sclep.ias.

Host plant

Mean total Mean percentMean length number of eggs of eggs

Number of of pupation per female hatchingani,mals (days) + SE

___SE

,4. curassaqAca

,4. syriaca

,4. incarnata

,4. tuberosa

12 10.31 105.7 ----. 8.7 91.6 4.9

17 10.67 117.2 + 1’0.6 89.1 + 5.7

12 11.02 110.3 --+ 9.4 87.3 + 6.3

9 10.57 106.0 +-- 9.6 93.2 +__ 4.8

’F.o5 (dr 3,20) 3. 0

F.ol (dr 3,20) 4.94

F- 1.13

F 0.73

concentrations (Duffey 197o, Singh and Rastogi I97O) and onlymarginally toxic (Hansen 1924, Heal et al. I95o). It is found,however, that contrary to expected results, larvae reared on thehighly toxic ‘4. curassavica gained more biomass per day, spent theshortest time in the 4th instar, and were the most efficient at utilizingand converting digested matter into bio.mass (Table 2). In addition,larvae reared on ,4. curassavica utilized approximately 65% of theassimilated energy to produce biomass whereas only 32% of theassimilated energy was allocated to biomass for larvae reared onA. t.uberosa (Table 3), and larvae reared on A. curassavica had thelowest ’Respiratory Coefficient’ at o.53 compared to larvae reared ond. tuberosa which had a value of 2.I6. This means that larvaereared on the ,4. curassavica host plant were allocating about 2calories for biomass for every calorie lost through respiration andmaintenance, whereas larvae reared on A. tuberosa allocated .ap-proximately o.5 calorie to biomass for every calorie 1,ost throughrespiration and maintenance. It thus .appears that there is littlemeasurable ’cost’ to detoxify or incorporate caridac g’tycosides bymonarch larvae since the larvae grew and developed most rapidlyon the most toxic ,4sclepias food plant tested.

1973"] Erickson Danaus #lexi##us 24.1

Recently, Brower et al. (972) have sho.wn a general decrease incardiac glycoside content of migrating monarch butterflies as thespecimens are collected farther south. They eel selection may beoperating against high cardiac glycoside content (larvae reared on. curassavica or A. humistrata) since, although high concentrationsot: cardiac glycosides in the butterfly coner greater protection rompredators, these authors surmise that these high concentrations de-crease the viability o.f the insect. In this experiment, there was no

significant difference in either the number of eggs deposited o.r thenumber of these that were ertile among the adult temales rearedon the four ,4sclepias species (Table 4). It does not appear at leastover a .couple o generations, that larvae reared on A. curassavica areany less viable than larvae reared on much less toxic Asclepias species.

The importance o.f nitrogen to.r larval growth and developmentcannot be overemphasized. House (96, x962) and Dadd (973)have discussed the qualitative requirements o, proteins and aminoacids or larval development. There appears to be an optimal nitro-gen level, which varies rom species to species, that produces maximallarval growth (Dadd 96, House x959, Vanderzant 958). Theecundity ot! Dacus dorsalis Hendel increased ’wifh an increase in theprotein content o the diet (Hagen I958), whereas low proteinlevels greatly prolonged the developmental period of Drosophilamelanogaster (Sang 956). In this experiment, larv.ae reared on

.4. tuberosa had the second astest developmental time of the 4groups o larvae, yet this ptant species contained a. little more thanone hal the nitrogen content in the leaves than was. contained inthe other leaves o.f the other host plants. Larvae o the monarchbutterfly appear, t’hereore, to have an adaptive strategy which al-lows them to best utilize a resource that is in limited supply. Al-though ’wasteful’ in the caloric sense, these larvae are able. to. securethe necessary supply o. nitrogen needed for the later adult stage byincreasing their total intake of food (Table 3). A similar situationhas been demonstrated in this laboratory involving the utilization ofcrucier plants by Pieris rapae (Slansky and Feeny, in preparation).This ability o an insect to compensate for decreased nutrient con-

tent of its food is discussed by House (965) and McGinnis andKasting (966). It thus appears that the low nitrogen content ofA. tuberosa has a somewhat limiting effect on the monarch larvaebut this low nutrient content only limits or regulates the efficiencywith which food is utilized by the larvae and does not limit thelarval growth or consumption rates to a significant degree.

:z42 Psyche [September

ACKNOWLEDGMENTS

The author wishes to thank Drs. L. P. Brower, P. P. Feeny andJ. G. Franclemont for reading the manuscript and offering helpfulsuggestions. Many thanks also go to, Ms. Sherry Rehr for technicalhelp and also offering suggestions on the manuscript. The work wassupported in part by Hatch Grant NY (C) 3943 of Dr. PaulFeeny.

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THE UTILIZATION OF SPECIES LARVAE PLEXIPPUSdownloads.hindawi.com/journals/psyche/1973/028693.pdf ·...

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Transcript of THE UTILIZATION OF SPECIES LARVAE PLEXIPPUSdownloads.hindawi.com/journals/psyche/1973/028693.pdf ·...