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Journal of the Lepidopterists Society 40(4), 1986, 255-263

SELECTIVE OVIPOSITION BY MONARCH BUTTERFLIES

(DANAUS PLEXIPPUS L.) IN A MIXED STAND OF

ASCLEPIAS CURASSAVICA L. AND A. INCARNATA L.

IN SOUTH FLORIDA

Stephen B. Malcolm and Lincoln P. Brower

Department of Zoology, University of Florida, Gainesville, Florida 32611

ABSTRACT. Host plant selection by ovipositing monarch butterflies occurred in a mixed stand of the milkweeds Asclepias curassavica and A. incarnata in a south Florida pasture. Three times more immature monarchs were found on A. curassavica than on A. incarnata. When these numbers were balanced for biomass differences between the two plant species, there were 5.7 times the number of monarch immatures/dry leaf mass/100 m2 on A. curassavica than on A. incarnata. Since A. curassavica had 36 times more cardenolide than A. incarnata, we suggest that the basis for selective oviposition by monarchs is to provide an effective cardenolide-based defense for their offspring.

Only 27 of the 108 North American species of the milkweed genus Asclepias (Woodson 1954) have been recorded as larval food plants of monarch butterflies, Danaus plexippus L. (Table 1). This restricted use of host species may reflect host availability, or active host selection. If, as Dixon et al. (1978) suggest, ovipositing monarchs do not discriminate between milkweed species on the basis of their cardenolide content, the criteria that determine patterns of resource use are likely to be based on the abundance, temporal and spatial distribution, and habitat diversity of different Asclepias species. On the other hand, Brower (1961) found that ovipositing female monarchs in south central Florida selected A. humistrata rather than nearby A. tuberosa plants. Such host selection may well be influenced by variations in leaf biomass and morphology, qualitative and quantitative chemical defenses, and nutritive value, between Asclepias species, as Price and Willson (1976) have suggested for another milkweed feeding specialist.

Recent observations near Gainesville, north Florida, in spring 1983 and 1984, indicate that monarchs do not lay eggs on the common milkweeds A. tuber osa and A. verticillata and rarely lay eggs on two less common species, A. amplexicaulis and A. tomentosa. These four species have low cardenolide concentrations and are medium-sized to small plants (Table 2; Roeske et al. 1976). Two other common milkweed species, A. humistrata and A. viridis, are heavily exploited by ovipositing females from early April to June (Malcolm et al. 1987). Interestingly, these two milkweeds contain the highest concentrations of cardenolides and have the largest leaf biomass of the available species in north Florida (Table 2). Since monarchs are well known for their ability to store milkweed-derived cardenolides as a defense against

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Table 1. North American Asclepias species serving as hosts of monarch butterfly larvae in nature.

Asclepias species

Reference

Brower (1961, 1962), Nishio (1980), Cohen and Brower (1982), Nishio et al. (1983), Malcolm et al. (1987)

Nishio (1980), Nishio et al. (1983)

Price and Willson (1979)

Wilbur (1976), Malcolm and Cockrell, unpubl.

Rawlins and Lederhouse (1981), Malcolm and Cockrell, unpubl.

Schroeder (1976), Malcolm and Cockrell, unpubl.

Beall (1948), Urquhart (1960), Malcolm and Cockrell, unpubl.

Barker and Herman (1976), Borkin (1982), Malcolm, Cockrell, Brower, and Brower, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Brower and Brower, unpubl.

Brower, Cockrell, and Malcolm, unpubl.

Lynch and Martin, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm, Cockrell, Lynch, and Martin, unpubl.

Brower, Cockrell, and Malcolm, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Brower (1961), this paper

Brower (1961), this paper

Malcolm and Cockrell, unpubl.

Brower and Brower, unpubl.

Riley, Lynch, and Martin, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Wilbur (1976)

Lynch and Martin, unpubl.

Malcolm and Cockrell, unpubl.

Malcolm and Cockrell, unpubl.

Brower, Cockrell, and Malcolm, unpubl.

Price and Willson (1979)

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Table 1. Continued.

Asclepias species

Location

Reference

predators (Brower 1984), cardenolides may be implicated in some form of host selection.

To test host selection by D. plexippus between Asclepias species, based on biomass and cardenolide measures, we counted the numbers of monarch eggs and larvae on plants within a mixed stand of two Asclepias species, A. curassavica and A. incarnata, that are known to have different cardenolide concentrations (Roeske et al. 1976).

Methods

The study site was a large mixed stand of A. curassavica and A. incarnata in a wet pasture adjacent to a man-made lake 15 km NW of Miami, Dade Co., Florida (25°45'N, 80°22'W, near junction of highways US-27 and 1-95). On 1 and 2 September 1984, six 10 m x 10 m, randomly selected plots were searched and the following measurements made: 1) number of plants per plot, 2) plant height, 3) number of stems per plant, 4) presence of flower buds and flowers (no seed pods were found), 5) number of leaf pairs per plant (like most milk-

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Table 2. Leaf cardenolide concentration and plant size of five milkweed species in May 1983 and 1984 within 25 km of Gainesville, Florida.

Cardenolide concentration (Mg/0.1 g dry leaf)

______________________________________________________________ Mean dry leaf

Asclepias species                      Mean                   SD                        Range                       N               biomass/plant (g)

Common

humistrata                   471              157              182-797              29                    7.8

viridis                           478              136             316-676                7                  12.5

verticillata                      14                — —                     1                 <0.1

Occasional amplexicaulis                   3                  3                 0-6                    4                    1.2

tomentosa                       15                12                  6-23                  2                    1.8

weeds these two species have opposite leaves), and 6) numbers of monarch eggs and larvae by instar. All eggs were collected and kept until larval emergence to determine whether they were D. plexippus or the queen, D. gilippus. The three eggs on A. curassavica and one on A. incarnata that proved to be queens were excluded from the analysis. Arbitrarily selected leaf samples were also collected from five plants of each species to measure leaf length, width and dry weight. These dried leaves were ground, mixed, and 0.2 g of each species extracted with ethanol to estimate their cardenolide concentrations by spectroas-say (Brower et al. 1975, 1984b).

Results

The cardenolide concentration of A. curassavica leaves was 864 /jig cardenolide/0.1 g dry leaf, and that of A. incarnata 24 fxg cardenolide/ 0.1 g dry leaf. Thus A. curassavica at this location had, on average, 36 times more cardenolide than A. incarnata.

The six 100 m2 plots contained 182 A. curassavica plants, with 430 stems on which 33 monarch immatures were found, and 77 A. incarnata plants, with 393 stems bearing 11 immature monarchs, distributed between the plots as shown in Table 3.

The two milkweed species are very similar in appearance, bearing similar sized, lanceolate leaves. Neither leaf length, width, or shape (length/width) of the two species were significantly different (Table 4a), but the dry leaves of A. incarnata were significantly heavier than A. curassavica. Since A. incarnata plants were significantly taller with more stems per plant than A. curassavica (Table 4a), they also had significantly more leaves (Table 4b). Thus each A. incarnata plant had greater biomass available to monarch larvae than A. curassavica. However there were more than twice as many A. curassavica than A. incarnata plants per 100 m2 (Table 4b), which resulted in similar num-

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Table 3. Distribution of immature monarchs on six 100 m2 plots in a mixed stand of A. cur assavica and A. incarnata near Miami, Florida, on 1 and 2 September 1984.

1        curassavica            34          92          6        —         2         —        —        —          8

1         incarnata              13          86          1        —        —        —        —         1           2

2        curassavica            62        162          6        —         1         —        —        —          7

2        incarnata              16          89        —        —        —        —        —        —          0

3        curassavica            17          44         1         —         1         —        —        —          2

3        incarnata                8          43        —        —         1         —        —        —          1

4        curassavica            31          69          5        —        —        —        —        —          5

4        incarnata                6          36          1        —        —        —        —        —          1

5        curassavica            17          27        —        —         1         —        —        —          1

5        incarnata              18          66        —        —         1         —        —        —          1

6        curassavica            21          36          4         3          2         —        —         1         10 6       incarnata              16          73          5        —         1         —        —        —          6

Total curassavica            182        430        22         3          7         —        —         1         33

Total incarnata                 77        393          7—         3         —        —         1         11

bers of stems overall (Table 3, t = 0.28, P = 0.78 NS) with almost equal leaf density and dry leaf biomass of each Asclepias species available to ovipositing monarchs (Table 4b).

Despite the similarity of the leaf biomass for each milkweed species, three times the number of immature monarchs (eggs to fifth instars) were found on A. curassavica than on A. incarnata (Table 4b). Similarly, when numbers of monarch immatures are corrected for host biomass, there were more than five times the number of monarch immatures/dry leaf mass on A. curassavica than on A. incarnata (Table 4b).

The difference between the numbers of monarch immatures on the two Asclepias species is unlikely to be explained by flower attraction since significantly more A. incarnata plants (with fewer monarch immatures) were flowering than A. curassavica (Table 4b), although most plants of both species were flowering.

Discussion

We suggest that our observation of significantly more immature monarchs/leaf mass on A. curassavica than on A. incarnata may be explained by the 36 times greater cardenolide concentration of A. curassavica over A. incarnata. These results contrast with those reported by Dixon et al. (1978) who suggest that monarchs oviposit on Asclepias species with the lowest cardenolide concentrations. They found that

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Table 4. Plant characteristics of A. curassavica and A. incarnata on six plots in a mixed stand at the study site near Miami, Florida, on 1 and 2 September 1984. Differences were tested at the 0.05 level.

D. plexippus laid more eggs on A. curassavica, with a cardenolide concentration of 56 Mg/0.1 g dry leaf, than on Gomphocarpus fruti-cosus, with 63 /*g cardenolide/0.1 g dry leaf. However, their cardenolide concentrations are too similar to reach any conclusion as to car-denolide-based oviposition preference, particularly as they are the same cardenolide determinations first reported as "approximate amounts ±50%" (Rothschild et al. 1975), and were not determined for the same plants used in their oviposition experiments. Gomphocarpus fruticosus is also an African milkweed species which casts doubt on experimental relevance, since monarch butterflies will only encounter recently introduced plants of this species in Australia. Using Australian D. plexippus, Zalucki and Kitching (1982) also found that females preferred to lay eggs on A. curassavica rather than on A. fruticosa (=G. fruticosus); but citing different published data on cardenolide concentra-

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tions (Roeske et al. 1976), they suggested the reverse, that monarchs laid eggs on the milkweed species with most cardenolide.

The use of milkweed-derived cardenolides appears to be at least a partial defense against wild avian predators for adult monarchs overwintering in Mexico (Fink & Brower 1981, Fink et al. 1983, Brower & Calvert 1985, Brower & Fink 1985). It is likely that monarchs in south Florida also benefit from cardenolide-based protection against bird predators, particularly as late summer bird migrants pass through south Florida.

Although we recently found that monarchs regulate their cardenolide concentrations by increasing or reducing the cardenolide concentrations from their larval host plants, milkweeds such as A. incarnata have insufficient cardenolide from which monarchs can concentrate an effective cardenolide-based defense. For example, although monarchs reared on A. speciosa can almost double their cardenolide concentrations relative to those of host plants, from 90 to 179 Mg/0.1 g (Brower et al. 1984b), this concentration is less than the concentrations in butterflies reared on other species of cardenolide-rich milkweeds. Roeske et al. (1976) found that adult monarchs reared from A. curassavica reflect the high cardenolide concentration of their host leaves, in this case of 386 Mg/0.1 g dry leaf, with a concentration of 319 jxg/ 0.1 g dry butterfly. In contrast, they found monarchs reared from A. incarnata with 0-28 [ig cardenolide/0.1 g had between 28 and 127 ng cardenolide/0.1 g dry butterfly. The emetic response of bird predators increases with cardenolide concentration above a lower threshold dependent on cardenolide polarity (Roeske et al. 1976). Thus monarchs that fed on A. curassavica as larvae at our site near Miami will be much better protected by cardenolides against bird predators than monarchs that developed on A. incarnata.

Since individual plants of both species have a mean dry biomass sufficient to support the development to pupation of at least one monarch larva (between 0.92 g and 1.74 g dry leaf is required [Schroeder 1976, Dixon et al. 1978]; A. curassavica has 0.034 x 35.21 = 1.20 g, and A. incarnata has 0.055 x 88.23 = 4.87 g [Table 4]) a monarch larva need not move from plant to plant, either within, or between the two milkweed species. Thus the effectiveness of cardenolide-based monarch defense is likely to be determined primarily by the oviposi-tion behavior of the adult female rather than by larval movements, particularly in view of the unpredictable costs and benefits of such larval movement between milkweeds (Borkin 1982). Unlike Borkin, we do not find instars 2 and 3 moving between plants in Florida. If late instars move between plants, they are more likely to find another A. curassavica plant. Their feeding experience may also ensure that they keep moving until they find another host plant of the same species.

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Cardenolides are unlikely to be the sole determinant of host selection in these observations. Other explanations of the observed oviposition bias for A. curassavica include 1) females may in some way be able to perceive a nutritional superiority of A. curassavica over A. incarnata (Erickson 1973); 2) monarch females may be more attracted to the orange and yellow flowers of A. curassavica than the pink flowers of A. incarnata (however, in central Florida monarchs preferred to oviposit on the pink flowered A. humistrata compared to the orange flowered A. tuberosa (Brower 1961, 1962)); and 3) females may have responded to the number of plants available for each species (Table 3) rather than to the similar quantities of stems, leaves, and leaf biomass.

Nevertheless, whatever the explanation, the natural experiment described in this paper as well as the observations reported by Brower (1961, 1962) are evidence for the oviposition preference by monarch butterflies for cardenolide-rich milkweed species. We suggest that this choice may be the result of natural selection having favored a discriminatory mechanism allowing adult female monarchs to choose milkweed species that provide their offspring with a more effective car-denolide-based defense against predators.

Acknowledgments

Jim Anderson and Andrew Brower helped collect the field data, and the paper was improved by the critical comments of Barbara Cockrell, M. P. Zalucki and an anonymous reviewer.

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