What Factors Affect Number of Eggs that Female Monarchs Lay?
(Continued)

Abstract  |  Background  |  Methods  |   Results  |  Discussion   |  Acknowledgments  |  References   |  Karen's Research Questions

Results

Summary of Lifetime Fecundity and Egg-Laying Lifespans

Total lifetime fecundity was extremely variable, ranging from 388-1224 in experiment 1, 114-965 in experiment 2, and 290-1179 in experiment 3. Egg-laying lifespan (the time from eclosion to the last day of egg laying) ranged from 11-33 in experiment 1, 11-32 in experiment 2, and 14-45 in experiment 3. The average number of eggs laid by females in all treatments and their egg-laying lifespan are shown in Table 1.

Table 1:  Mean fecundity and lifespan in each experiment.

Treatments in experiments 1 and 3 refer to the sizes and numbers of spermatophores received (e.g. large = one large spermatophore; large, small = a large spermatophore followed by a small spermatophore; etc.). In experiment 2, MM = multiple mating treatment, SM = single mating treatment, low feed = 15% honey water concentration, high feed = 30% honey water concentration.

I tested whether a female’s total fecundity was influenced by the amount of spermatophore material she received during mating, the concentration of food she was given, her egg-laying lifespan, or her size (as measured by her mass one day after she eclosed). I also tested whether her lifespan varied with her size, feeding treatment, or mating treatment. In both cases, I used linear regression analyses (table 2). In experiment 1, none of the factors I measured influenced either fecundity or lifespan. In experiment 2, females that laid eggs over a longer period of time and those that were in the multiple mating treatment, tended to lay more eggs (table 2). There were no effects of female mass at eclosion or feeding treatment on fecundity, nor did any of these factors affect female lifespan. In experiment 3, females that laid eggs over a longer period of time and those that received a large first spermatophore tended to lay more eggs (figure 3), and larger females tended to live longer (table 2). The effects of lifespan on fecundity, and female size on lifespan in experiment 3 are illustrated in figures 2a and b.

Table 2:  Predictors of fecundity and lifespan in experiments 2 and 3

Daily Fecundity

In all three experiments, fecundity peaked during the first week of egg-laying, then gradually decreased. This pattern is illustrated in Figure 3, which also shows the effect of first spermatophore size.  Part of the variation in daily fecundity is due to ambient conditions; females lay few eggs on cool or rainy days, and many on warm, sunny days. The maximum number of eggs laid by one female on a single day was 205, laid on the fifth day of oviposition by a female in experiment 3.

Even though females laid very few eggs per day at the ends of their egg-laying lives, all females in experiment 3 had oocytes remaining at the end of their egg-laying life. The number of mature oocytes in an intact ovariole ranged from three to 15, meaning that the total number of mature oocytes in all eight ovarioles ranged from approximately 24 to 120. This number did not vary with mating treatment, female size, or lifespan. Females also had immature oocytes in the distal ends of the ovarioles (see oogenesis). All females had either no or few fat bodies remaining in their abdomens.

Female mass

Female mass decreased with age in both years that I measured their masses throughout their lives. In experiment 2, females in the multiple mating treatment lost mass more slowly and females that received the 30% honey solution consistently weighed more. In 1994, females that received one small spermatophore lost mass more rapidly than other females and those that received two large spermatophores lost mass more slowly.   These analyses only included masses during the time females were laying eggs. After this, those that were still alive often gained mass because they were no longer able to fly and did not lay eggs, but were still being fed every day. In fact, many females became obese; one weighed 946 mg, or 1.78 times her initial mass, on her last weighing.

By the end of their egg-laying lives, females in both years weighed about 88% of their initial mass (1994 mean 87.7%, s.e. = 2.5%; 1988 mean 87.9%, s.e. = 3.2

Discussion

Effects of female mass on lifespan and fecundity

If we assume that female mass is a measure of nutrients received as larvae, the analyses of both fecundity and mass changes suggest that female monarchs use larval reserves for somatic maintenance, but not to increase egg production. There was a positive correlation between lifespan and size in 1994; larger females lived longer. However, there was no correlation between size and lifespan in experiments 1 and 2. Possible explanations for this include lower variation in female size in the 1986 experiment, and the extremely hot weather conditions in 1988 that shortened lifespans and may have counteracted the beneficial effects of additional larval reserves. Mass loss data provide additional evidence that larval reserves are important for somatic maintenance. Females lost an average of 12% of their mass in both 1988 and 1994, despite laying eggs over a longer period in 1994.  It appears that females lay eggs as long as they have the reserves to support oviposition activity. I only dissected females after they died in 1994, but these females had little fat and many eggs remaining at the ends of their lives. This supports the conclusion that females quit laying eggs, but not producing them, when they run out of larval reserves.

Although female size and fecundity were positively correlated in 1994, large females lived longer, and controlling for lifespan made the effect of size insignificant (Table 2a). In 1988, there was no relationship between female size and fecundity. However, larval reserves do affect female reproductive success, despite the lack of a direct connection between female mass and fecundity. In captive monarchs, the ability to lay the eggs that are produced, and not egg production itself, appears to be the limiting factor in realized fecundity; females run out of reserves needed for maintenance when they have many eggs unlaid.

Effects of adult income on fecundity

The large reproductive output of female monarchs indicates that much of the material used in eggs comes from adult income. The egg mass produced by females was the equivalent of about 70% of their initial body mass (see How big are monarch eggs?, Oberhauser 1997), but they only lost about 12% of their body mass over the course of egg laying.

Because the adult diet of many Lepidoptera consists of nectar (a poor source of protein), ingested nutrients in these species should be less important to fecundity than the protein-rich spermatophores (Boggs 1979, Marshall 1982, Oberhauser 1992, Bissoondath & Wiklund 1995) received from males. I found no effect on fecundity with a two-fold difference in the concentration of honey-water in 1988, even though females that received the higher concentration weighed more and thus must have ingested more calories. Other researchers have found effects of the adult diet of nectar-feeding Lepidoptera on fecundity, but in several of these studies lower fecundity occurred when females were given no carbohydrates at all (Norris 1935, David & Gardiner 1962, Murphy, Launer & Ehrlich 1983, Karlsson & Wickman 1990). When Boggs & Ross (1993) gave Mormon fritillary females either one half or one third the volume of honey water consumed by females fed as much as they would eat, fecundity also decreased. Likewise, common crow butterfly (Hill 1989) and common imperial blue (Hill & Pierce 1989) females laid more eggs when they received 25% vs. 1% sugar solutions. These results suggest that a certain amount of carbohydrates from the adult diet is needed for females to realize maximum fecundity. My feeding regime provided this amount, whereas others summarized above did not.

Unlike nutrients from the adult diet, male-derived nutrients do affect fecundity in monarchs. Females that received a large spermatophore early in experiment 3 or were allowed to mate multiply throughout the egg-laying period in experiment 2 showed increased fecundity. It appears that male-derived nutrients are used relatively quickly after receipt, and not saved for later use. Multiply mating females in experiment 2 were allowed to mate at three day intervals throughout their lives, while those in experiment 3 mated only twice early in egg laying. Differences between the mating treatments in experiment 2 were apparent throughout the egg laying period (Oberhauser 1989), whereas after about ten days of egg laying there were no differences between females that received large or small first spermatophores in experiment 3 (figure 3). Spermatophores are completely broken down within one to seven days after mating (Oberhauser 1992) and the nutrients they contain are incorporated into eggs almost immediately (Boggs & Gilbert 1979, Wells et al. 1993).

Other researchers have found that female butterflies and moths that mate multiply use nutrients obtained during mating to increase fecundity (Rutowski, Gilchrist & Terkanian 1987, Watanabe 1988, Wiklund et al. 1993, Tamhankar, Gothi & Rahalkar 1993, Tamhankar 1995, Ward & Landolt 1995). In single mating species, on the other hand, varying the amount of male-derived nutrients that females receive rarely affects fecundity (Greenfield 1982, Jones et al. 1986, Svärd & Wiklund 1991). These studies of single mating species have been interpreted as contradictory to studies that did show an effect of male derived nutrients on fecundity. However, it might be that we should not expect this effect in monandrous species. A possible explanation for the difference between the results of studies of monandrous and polyandrous Lepidoptera is that it is possible to set up experiments with more variation in the amount of male-derived nutrients when females mate multiply. Another explanation is that monandrous females have not evolved to utilize male-derived nutrients to make eggs. Once this occurs, there should be strong selection pressure for females to mate multiply.

Effects of adult income on lifespan

Female monarchs do not appear to use adult income, either from their food or from males, to increase their lifespan, at least within the ranges of income provided in these experiments. Females that received a higher concentration of honey water in experiment 2 did not live longer, and increased male-derived income did not increase lifespans in either year.

Two studies of single mating Lepidoptera also showed no effect of spermatophore size on female lifespan (Royer & McNeil 1993, Svärd & Wiklund 1991). However, in three multiply-mating species, females that received more male-derived nutrients lived longer (Rutowski et al. 1987, Wiklund et al. 1993, Tamhankar 1995). These studies provided more variation in the number of spermatophores received than experiment 3, and it is possible that my treatments were not different enough to allow detection of such an effect. In experiment 2, there were larger treatment differences, but the severe weather conditions during the summer of 1988 may have negated any effects. The fact that Boggs and Gilbert (1979) found male-derived nutrients in female somatic tissue as well as eggs suggests that such an effect is possible, and my results can not rule out a relationship between lifespan and male-derived nutrients under a different test regime.

In nectar-feeding Lepidoptera, completely withholding sugar from the adult diet shortens lifespans (Norris 1935, David & Gardiner 1962, Murphy et al. 1983, Karlsson & Wickman 1990), as does providing a 1% sugar solution (Hill 1989, Hill & Pierce 1989). However, when female Mormon fritillaries were fed one half or one third as much of a 25% honey solution as that eaten by females fed as much as they would eat, there was no effect of feeding treatment on lifespan (Boggs & Ross 1993). These studies, in combination with the work described here, indicate that nectar-feeding Lepidoptera need to obtain some sugar as adults to realize a full lifespan, but there is probably a threshold amount, over which no additional benefits are realized.

Conclusion

Female monarchs appear to use increased amounts of male-derived income to increase egg production, and may use increased larval reserves to increase their lifespan. However, realized fecundity is affected by both egg production and the time over which females lay eggs, so both larval reserves and adult income are important to female fitness. In fact, females appear to run out of the reserves used for somatic maintenance before egg production terminates.

Acknowledgements

I thank De Cansler, Ann Feitl, Rachel Hampton, Brenda Jenson and Christine Jessup for all of their help counting and weighing eggs. Don Alstad, Carol Boggs and Christer Wiklund provided helpful comments on an earlier versions of the manuscript. This study was funded by the National Science Foundation (DEB-9220829 and DEB-9442165).

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