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James M. Erickson.
The Utilization of Various Asclepias Species by Larvae of the Monarch Butterfly, Danaus plexippus.
Psyche 80(3):230-244, 1973.

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THE UTILIZATION OF VARIOUS ASCLEPIAS SPECIES BY LARVAE OF THE MONARCH BUTTERFLY,
DANA US PLEXIPPUS
BY JAMES M. ERICKSON*
Dept, of Entomology, Cornell University
Ithaca, New York, 14850
Plants of the genus Asclepias are well known to contain high concentrations of cardiac glycosides
(cardenolides) . It is generally
surmised that such cardiac stimulants function to protect plants containing th,em against insect and vertebrate herbivores (Euw et al. 1967). In addition, some insects which are adapted to feed on Asclepias plants store cardiac glycosides apparently as a means of protection against vertebrate predators which find the compounds distasteful (Brower and Brower 1964, Brower 1969). It was by means of such an herbivore-predator interaction, bluejays feeding on monarch butterflies, Danaus plexippus L. ( Brower I 969, Brower et al. 1968), that a spectrum of palatability was detected among monarch butterflies reared on various species of milkweed. It is surmised that this spectrum of toxicity to a vertebrate predator reflects a spectrum of concentrations of cardiac glycosides in the different species of the insects' larval food plants (Brower and Brower 1964, Brower et al. 1967, Brower 1969). However, quantitative and qualitative data for cardenolides in Asclepias leaves are at best in- complete (Reynard and Morton 1942, Kupchan et al. 1964, Duffey 1970, Singh and Rastogi 1970, Feir and Suen 1971, Duffey and Scudder 1972, Scudder and Duffey 1972, and Eggermann and Bongers 1972).
The following experiments were undertaken to determine wheth'er a differential response by D. plexippus larvae to their host plants could be detected by measuring their efficiency of food utiliza- tion and whether such a response would support the concept of a spectrum of toxicity. It seemed conceivable that detoxication or storage of cardiac glycosides might require expenditure of energy and could be detected by a lowered f'eedine efficiency. In addition, -
Brower et al. (1972) 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 IS, 1973.



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general viability of monarch adults which have stored higher con- centrations of cardiac glycosides. To test this hypothesis the fertility and fecundity of adult monarchs was determined. Groups of intact larvae of D. plexippusl were taken from the second generation of a culture founded from wild insects taken near Ithaca, New York, and were reared in the laboratory on one of the following species of Asclepid host plants : A. curassavica, A. synaca, A. incarnata, or A. tuberosa. Newly molted 4th-instar larvae were placed individually in glass petri dishes (Pyrex, 1oomm X 15mm) lined on the bottom with a piece of Whatman No. I filter paper. Mature and uninjured leaves of the native species were gathered in the field each day from plants growing in open sunlit areas, and leaves of A. curassavica were collected from plants grown in the greenhouse. All leaves were sealed in plastic bags and used within 2 hours. These randomly collected leaves were split along the mid- rib, one half weighed and offered to the larvae and the other half used to determine the percent dry matter in the leaf material ( Waldbauer I 960, I 964) . Leaves were replaced and feces collected every 24 hours.
All the larvae were placed in a controlled temperature room, except for the period of time each day during which new food was offered to the larvae and the feces collected. The room was kept
relatively constant with day-night temperatures of 22' and 18O, 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 ( I 960, I 964), except that plant material was lyophilized instead of oven-dried. The dry weight of the food utilized or assimilated was assumed to be the dry weight of the food ingested minus the dry weight of feces. An additional group of larvae was reared along with the experimental larvae, and these were sacrificed to determine the dry weights, and thus, the per- centage dry matter of the larvae. Indices of food utilization were determined following the methods of Waldbauer ( I 960, I 964, 1968). Many terms have been used both by ecologists and by physiologists to describe various measures and indices of food Specimens of the insects used in this research have been deposited in the Cornell University Insect Collection, Lot 1023, Sublot 14. Specimens of the plants have been deposited in the Bailey Hortorium, Cornell University.



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232 Psyche [September
utilization and efficiency. Relationships between many of these terms are discussed by Kozlovsky ( I 968) and Waldbauer ( 1968). 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, 1971 ) or the 'Coefficient of Di- gestibility' (Waldbauer 1964, 1968, House 1965)) was used. In practice, this measure is only an approximation since the numerator (as determined by the standard gravimetric technique) does not quite represent the amount of food actually assimilated (Waldbauer 1968). This slight error is due to the presence of metabolic wastes in the feces in addition to the undigested food (Lafon 1951 ), but Hiratsuka (1920) and Waldbauer (1964, 1968) point out that this difference between true and measured assimilation efficiencies is negligible.
The efficiency with which ingested food is converted to biomass is calculated by dividing the dry weight of food ingested into the dry weight gained by the larva. This index, referred to by physiolo- gists as the 'Efficiency of Conversion of Ingested Matter' (Wald- bauer 1968) and by ecologists as the 'Ecological Growth Efficiency' (Odum 1971)) is an overall measure of an animal's ability to utilize for 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 the dry weight gained by thle larva. This index, referred to by Wald- bauer ( I 968 ) as the 'Efficiency of Conversion of Digested Matter' and by Odum ( 1971) as the 'Tissue Growth Efficiency', decreases as the proportion of digested food metabolized for energy and main- tenance of physiological functions increases (Waldbauer 1968). The relative growth rate is calculated by dividing the mean dry weight of the larva times the duration of the instar in days into the dry weight gained by the larva during the stadium (Waldbauer 1968). This index reflects the rate at which biomass is added by a larva corrected for any size differential between groups of larvae. The 'Respiratory Coefficient' (Lindeman I 942) is described as the ratio of respiratory and maintenance loss to the net secondary production or biomass increase. This coefficient is calculated by dividing the total calories lost through respiration and maintenance by the total calories added to the insects' biomass. This ratio is what may be termed an 'Energy Production Cost Ratio'; the smaller the coefficient or ratio, the morte efficient the larva is at allocating energy to biomass, the larger the coefficient, the greater the number



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of calories lost through respiration and maintenance per calorie allocated to biomass.
Of general interest to ecologists is the 'Principle of Allocation' described by Cody ( 1966). Organisms have a limited amount of energy to spend and will be selected to partition this energy in dif- ferent ways depending upon changing physiological or environmental conditions. Any activity of an organism, or more precisely, the energy expenditure for that activity, can be viewed only in relation to all other demands for energy. To descry any increased 'cost' of detoxifying or incorporating cardenolides by D. plexippus larvae when reared on Asdep'ias host plants with known toxicity spectrum, a larval energy budget based on dry weights was constructed. Calo- rific values of the larval food plants, feces and larvae were deter- mined by means of a Phillipson non-adiabatic microbomb calorimeter (Gentry and Wiegert Inst. Inc., Aiken, C.S.) (Phillipson 1964). The Iyophilized plant material was subjected to five replications whereas lyophilized larvae and feces were subjected to three replica- tions for the determination of calorific values. The nitrogen content of the leaf material was determined by the Kjeldahl method for total nitrogen (Williams 1964). A minimum of three replicate samples were obtained for each of the plant species. For the purposes of food utilization and efficiency determinations, the experiment was concluded den the larvae minted into the ultimate instar. The larvae were then reared through to the adult stage on the same experimental plants that they fed upon in the utilization experiments. All adult females were hand paired and placed individually in a I meter square screen cage with one A. curassavica and one A. syriaca plant of approximately the same age and condition. Records were kept each day of the number of eggs laved per female 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 various experimental parameters and indices were subjected to one-way analysis of variance to determine differences in efficiencies or develop- mental rates among the various larval food plants. Various plant parameters differed greatly among the four Asclepicss species offered to the monarch larvae (Table 1). The leaves of A, tuberosa were significantly higher in dry matter content than the other three species, No significant difference in caloric content could



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Psyche
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be found among the four Asclepias species. The nitrogen content of thle leaf material did not vary significantly for A. curassavica, A. syriaca, and A. incarnata but the leaves of A. tuberosa contained a little more than one half the total nitrogen content of the other plants examined.
The proportion of ingested food which was digested and as- similated ('assimilation efficiency') averaged about 50% for all experimental host plants except for A. syriaca which was signifi- cantly higher (P<o.05) with a mean of approximately 58 % (Table 2). The efficiency with which ingested matter was con- verted to biomass ranged from 29.59% for larvae reared 011 A. syriaca to 16.39% for larvae reared on A. tuberosa (P<o.oI), whereas the efficiency of conversion of digested matter ranged from 53.30% for larvae reared on A. curassavica to 34.04% for larvae reared on A. tuberosa (P<o.oI). The duration of the 4th stadium also varied significantly ( P < 0.0 I ) with larvae on A. cz~rassavica having the shortest duration (2.15 days) and larvae on A. syriaca having the longest duration (2.55 days). The amount of biomass gained per day per larva also varied significantly ( P < 0.05) with larvae reared on A. curassavica gaining the most weight (16.42 mg/day) and larvae on A. incarnata the least ( 12.70 mg/day). Of great interest, however is that the relative growth rate did not vary significantly for the larvae feeding on the four Asclepias species. The total allocation of energy by the larvae on tlie different host plants can be found in Table 3. The larvae reared on A. tuberosa ingested and assimilated almost twice as many calories as larvae reared on A. curassavica or A. syriaca. The total number of calories allocated to larval biomass did not vary to any extent among the Asclepias species; ingestion of more calories by larvae reared on A. incarnata and A. tuberosa was balanced by greater costs for res- piration and maintenance. The ratio of the total number of calories allocated to an increase 'in 'larval biomass to the total calories assimilated ranged from approximately 65% by larvae reared on A. curassavica to approximately 32% for larvae reared on A. tuber- om. The respiratory coefficient also ranged from 0.53 (A. curas- savica) to 2.16 (A. tubcrosa) .
There was no difference in the mean length of the larval stage or the pupal stage among larvae reared on the various Asclepias species (Table 4). Larval survival was 100% on all host plants except A. incarnata where 90% of die larvae survived to the adult stage. Fecundity and fertility does not vary significantly; the mean number of eggs layed per female ranged from 103.7 for females reared on



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Assimilation
efficiency
TABLE 2.
The utilization of food by 4th-instar larvae of the monarch butterfly, D. plexippus, when reared on various species of Asclepias food plants (Mean k SE). A. curassavica A. syriaca A. incarnata A. tuberosa F* Efficiency of conversion 28.69 k
of ingested matter 1.23
Efficiency of conversion
53.30 =k
51.83 k 44.99 2
of digested matter
2.15 2.58
1.41
Relative growth
rate
Duration of 4th
stadium (days)
Larval biomass gain
16.42 k
14.09 k
12.70 * 13.17 * 4.23
(mg dry weight/day)
1.56 0.96
1.17 1.21
*F.o5 (df 3,28) = 2.96
F.oi (df 3,28) = 4.62




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Erickson - Danaus plexippus
A. curassavica to I 17.2 for females reared on A. syriaca. The mean per cent of eggs hatching ranged from 87.3% (A. incwnato) to
93.2% (A. tuberosa) .
One of the major concerns of modern ecology is the description and explanation of the energetic relationships between and within various communities. A knowledge of the food utilization efficiency of insects is thus of particular importance to ecology since insects exert a substantial influence and impact on almost all terrestrial or fresh water communities. The ecological significance of such energy utilization studies have been extensively reviewed ( Englemann I 966, Phillipson I 966, and others).
It seems apparent that adaptive nutritional differences in host plants must be sought on a quantitative levlel and that meaningful comparisons of food utilization and nutrition will not emerge until quantitative studies are carried out. The determination of absolute requirements for dietary constituents depends upon the measurement of food or nutrient intake. Differences in food efficiency can be demonstrated only be measuring intake and growth. Measurement of the food intake and the utilization of this food elucidates to a great degree the physiological processes occurring in an insect since patterns of utilization may be different although food sources are similar in their ability to support growth. For instance, low food intake may be offset by a high utilization of ingested or digested food and a very high food intake may well lead to a very low efficiency in the utilization of ingested or digested matter. In this experiment, the assimilation efficiency of the larvae did not vary significantly among the various AscZepias host plants except for larvae reared on A. syriaca which had an efficiency about 8% higher than larvae on thce other host plants. This means that the larvae reared on the various host plants were digesting and excreting ap- proximately equal amounts of food. The efficiency with which ingested food and digested food are utilized varied significantly with larvae reared on A. curassavica and A. syriaca having the highest efficiencies and larvae reared on A. tuberosa the lowest (Table 2). The efficiency with which digested food is utilized for growth will vary not only with the maintenance and respiration requirements for energy but also with the balance of nutrients in the food source. Larvae reared on A. tuberosa ingested almost twice as much food during t'he 4th instar as larvae reared on the other three host plants



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FABLE 3.
The allocation of energy during the 4th-instar by the larvae of the monarch butterfly, D. plexippus, reared on various Asclepias host plants. Mean total Mean total
calories calories Mean total Calories
Calories to
metabolic
Respiratory
coefficient
ingested egested calories to Percent of and Percent of (Lindeman, Plant Species (food) (feces) assimilated biomass assimilated other losses assimilated 1942) 2
'^i
r^
A. syriaca 569.37 228.18 341.19 189.66 55.58 151.53 44.42 0.80 ,4. tuberosa 961.56 442.90 5 18.66 164.05 31.62 354.61 68.38 2.16



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19731 Erickson - Danaus plexippus 239
(see Table 3). As the ingestion rate increases, there is a negative correlation with the efficiency with which ingested or digested matter are utilized (Waldbauer 1968). This reduction in overall gross and net efficiency has been shown for Prodenia larvae (Soo Hoo and Fraenkel I 966)
and by House
( I 965 ) . The larvae reared on A.
tuberosa may be viewed as being extremely 'wasteful' of the potential caloric content of their food, most likely passing great quantities of food through the digestive tract to secure a supply of some limiting nutrient or substance. The leaf material does not vary to any sig- nificant degree among the Asclepias species tested in terms of caloric content (Table I ) , whereas the leaves of A. tuberosa contain a little more than one half the nitrogen content of the other three species. It has been suggested that the water content of food material will greatly affect the utilization of this material. It is generally the case with the swallowtail butterfly, Papilio polyxenes, that the efficiency of utilization of food decreases as the dry matter content of the food plant increases (Erickson and Feeny, in preparation). In this ex- periment, there is a significant difference in the dry matter content of the leaves, with A. tuberosa having the highest dry matter con- tent at approximately 21% and A. incarnata and A. syriaca the lowest dry matter content at about 17%
(Table I). It has been
shown in this laboratory, that by varying the water content of leaf material, the utilization of food by the cecropia moth, Hyalophora cecropia is greatly affected (J. M. Scriber, in preparation). The effect is shown not in an increased intake rate, as occurs in monarch larvae, but in lengthened larval development times, in which the total food intake is increased but the rate of this intake remains relatively constant. It thus appears that the dry matter content of Asclepias leaves may have some influence on the utilization efficiencies but not to the degree found in this experiment. In keeping with Cody's (1966) 'Principle of Allocation', I at- tempted to descry any increased 'cost' for D. plexippus larvae to detoxify or to incorporate cardenolides. It is well known that A. curassavica is highly toxic and contains at least 15 cardenolidies (Kupchan et al. 1964, Duffey 1970), three of which have been isolated from distasteful D. plexippus larvae (Parsons 1965, Reich- stein 1967) incorporated there as a defense against vertebrate preda- tors (Brower and Brower 1964, Browei- et al. 1967, Brower 1969). Asclepias syriaca has been found to be only slightly toxic to verte- brates and to contain at least seven cardiac glycosides (Reynard and Morton 1942, Duffey 1970, and others). Asclepias incarnat~ and A. tuberosa are known to contain cardenolides but in much, lower



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240 Psyche
[September
TABLE 4. Length of pupation, fecundity and fertility of monarch butterflies raised on various plants of the genus Asclepias. Mean total Mean percent
Mean length number of eggs
of eggs
Number of of pupation
per female
hatching
Host plant animals (days) SE12 SE1
A. curassawica 12 10.31
105.7 zk 8.7 91.6 2 4.9
A. syriaca 17 10.67 117.2 2 10.6
89.1 5.7
A. incarnata 12 11.02
110.3 & 9.4 87.3 k 6.3
A. tuberosa 9 10.57
106.0 31 9.6
93.2 4.8
lF.05 (df 3,20) = 3.10
F.01 (df 3,20) = 4.94
'F = 1.13
'F' = 0.73
concentrations (Duffey 1970, Singh and Rastogi 1970) and only marginally toxic (Hansen 1924, Heal et al. 1950). It is found, however, that contrary to expected results, larvae reared on the highly toxic A. curassavica gained more biomass per day, spent the shortest time in the 4th instar, and were the most efficient at utilizing and converting digested matter into biomass (Table 2). In addition, larvae reared on A. curassavica utilized approximately 65% of the assimilated energy to produce biomass whereas only 32% of the assimilated energy was allocated to biomass for larvae reared on A. tuberosa (Table 3), and larvae reared on A. curassavica had the lowest 'Respiratory Coefficient' at 0.53 compared to larvae reared on A. tuberosa which had a value of 2.16. This means that larvae reared on the A. curassavica host plant were allocating about 2 calories for biomass for every calorie lost through respiration and maintenance, Whereas larvae reared on A. tuberosa allocated ap- proximately 0.5 calorie to biomass for every calorie lost through respiration and maintenance. It thus appears that there is little measurable 'cost' to detoxify or incorporate caridac glycosides by monarch larvae since the larvae grew and developed most rapidly on the most toxic Asclepias food plant tested.



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19731 Erickson - Dmaus plexippus 241
Recently, Erower et al. (1972) have shown a general decrease in cardiac glycoside content of migrating monarch butterflies as the specimens are collected farther south. They feel selection may be operating against high cardiac glycoside content ( larvae reared on A. curassavtca or A. humistrata) since, although high concentrations of cardiac glycosides in the butterfly confer greater protection from predators, these authors surmise that these high concentrations de- crease the viability of the insect. In this experiment, there was no significant difference in either the number of eggs deposited or the number of these that were fertile among the adult females reared on the four Asclepias species (Table 4). It does not appear at least over a couple of generations, that larvae reared on A. curassmica are any less viable than larvae reared on much less toxic Asclepias species. The importance of nitrogen for larval growth and development cannot be overemphasized. House ( 1961, 1962) and Dadd (1973) have discussed the qualitative requirements of proteins and amino acids for larval development, There appears to be an optimal nitro- gen level, which varies from species to species, that produces maximal larval growth (Dadd 1961, House 1959, Vanderzant 1958). The fecundity of Dacus dorsalis Hendel increased with an increase in the protein content of the diet (Hagen 19581, whereas low protein levels greatly prolonged
the developmental period of Drosophila
melanoguster (Sang 1956).
In this experiment, larvae reared on
A, tubfroso had the second fastest developmental time of the 4 groups of larvae, yet this plant species contained a little more than one half the nitrogen content in the leaves than was contained in the other leaves of the other host plants. Larvae of the monarch butterfly appear, therefore, to have an adaptive strategy which al- lows them to best utilize a resource that is in limited supply. M- though 'wasteful' in the caloric sense, these larvae are able to secure the necessary supply of nitrogen needed for the later adult stage by increasing their total intake of food (Table 3). A similar situation has been demonstrated in this laboratory involving the utilization of crucifer plants by Pieris rapae (Slansky and Feeny, in preparation). This ability of an insect to compensate for decreased nutrient con- tent of its food is discussed by House (1965) and McGinnis and Kasting (1966). It thus appears that the low nitrogen content of A. tuherosa has a somewhat limiting effect on the monarch larvae but this low nutrient content only limits or regulates the efficiency with which food is utilized by the larvae and does not limit the larval growth or consumption rates to a significant degree.



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Psyche
[September
The author wis8hes to thank Drs. L. P. Brower, P. P. Feeny and J. G. Frandemont for reading the manuscript and offering helpful suggestions. Many thanks also go to Ms. Sherry Rehr for technical help and also offering suggestions on the manuscript. The work was supported in part by Hatch Grant NY (C) 139413 of Dr. Paul Feeny.
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19731 Erickson - Danaus plexippus 243
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244 Psyche [September
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