The slow-growth-high-mortality hypothesis proposes that increased development time in arthropods feeding on suboptimal food may result in an increased vulnerability to natural enemies. We measured the development time of the forest caterpillar Orgyia leucostigma J.E. Smith (Lepidoptera: Lymantriidae: Orgyiini) on two of its host plants and used a 7-year database on parasitism of this species to test the slow-growth-high-mortality hypothesis. We found that female O. leucostigma developed faster when fed on willow (Salix nigra Marsh) than when fed on box elder (Acer negundo L.). However, only one of the parasitoids of the parasitoid community that attack these larvae followed the prediction of the slow-growth-high-mortality hypothesis. Overall parasitism of O. leucostigma on willow was greater than in box elder, contradicting the slow-growth-high-mortality hypothesis prediction. This is the first test of the hypothesis to consider parasitism by several species in the parasitoid community attacking a free-feeding herbivore on two distantly related plant species.
An increased development time in arthropods due to feeding on suboptimal food is a relatively common phenomenon (Slansky & Feeny, 1977; Barbosa et al., 1983; Denno et al., 1990; Kaspi et al., 2002). In contrast to individuals feeding on optimal diets, individuals feeding on poor quality food not only have an extended development time but may be vulnerable to natural enemies. That is, the probability of mortality due to natural enemies is likely to be greater because of the prolonged period of vulnerability (Feeny, 1976; Price et al., 1980). These ideas were formalized in the ‘slow-growth-high-mortality’ hypothesis, which states that the prolonged larval development of herbivores results in a greater vulnerability and thus a greater mortality due to natural enemies (Clancy & Price, 1987).
Häggström & Larsson (1995) found that Galerucella lineola F. (Coleoptera: Chrysomelidae) developed more slowly, grew less, and were subject to predation when feeding on Salix dasyclados Wimmer to a greater degree than when feeding on Salix viminalis L. These results supported the prediction of the slow-growth-high-mortality hypothesis. Similarly, Pieris rapae L. (Lepidoptera: Pieridae) larvae feeding on collards containing low nitrogen levels took longer to develop and were subjected to greater predation by invertebrate predators than rapidly developing larvae feeding on high nitrogen collards (Loader & Damman, 1991). Furthermore, cohorts of the late hatching tent caterpillar, Malacosoma disstria Hübner (Lepidoptera: Lasiocampidae), feeding on late (i.e., poor quality) trembling aspen (Populus tremuloides Michaux) budbreaks, developed slower and were subject to more predation than early hatching caterpillars feeding on early (i.e., good quality) budbreaks (Parry et al., 1998). All these studies focused on the effect of herbivore food quality on predators. Although informative, estimates of predation can be confounded by the dispersal or disappearance of herbivores from plants due to other unknown factors (Medina & Barbosa, 2003). Estimates of parasitism constitute a relatively more accurate evaluation of natural enemy-inflicted mortality than estimates of predation.
Most free-feeding insects experience attack by several species of parasitoids and thus studies on the effect of parasitoid communities on an herbivore might produce a valid assessment of the ecologically relevant effect of slow growth on parasitoid-inflicted mortality. However, there have been no studies analyzing the effect of the parasitoid community on a free-feeding herbivorous insect. In this study we have compared the development of the macrolepidopteran Orgyia leucostigma J.E. Smith (Lepidoptera: Lymantriidae) on two of its host plant species. We then used this data, and data on parasitism by the parasitoid assemblage attacking this forest caterpillar, to test the slow-growth-high-mortality hypothesis.
Most forest caterpillars occur in very low numbers (Barbosa et al., 2000). In Maryland, O. leucostigma is one of the relatively abundant species of caterpillars in riparian forests. It is also a very polyphagous species (Barbosa et al., 2003). Collections started in 1991 (by P.B.) of all the Macrolepidoptera on willow and box elder have generated a 7-year data set on caterpillar abundances and levels of parasitism (Barbosa et al., 2001). General rearing of larvae during this study suggested that willow and box elder might differ in their suitability for O. leucostigma. In particular, box elder seemed less suitable than willow. However, this difference was not rigorously determined, nor are there any studies comparing the development of O. leucostigma on two host plants under identical conditions. In this study we compared the development and adult mass of O. leucostigma on two tree species and used our 7-year database to calculate and compare the percentage parasitism of O. leucostigma on both willow and box elder in order to test the slow-growth-high-mortality hypothesis.
Materials and methods
Orgia leucostigma, the white-marked tussock moth, is a common polyphagous species throughout the eastern deciduous forests of North America, and it feeds on the foliage of a large number of species in various tree genera (Johnson & Lyon, 1976). Orgia leucostigma egg-masses were obtained in the laboratory by mating moths collected from two common tree species, willow and box elder, at several sites across Maryland (see Barbosa et al., 2000 for site descriptions). The willow and box elder trees shared the same habitats but were at least 20 m apart from each other in all our sites. Orgyia leucostigma egg-masses were kept in a growth chamber at 28 °C and 75% r.h. with a L16:D8 photoperiod. As soon as larvae eclosed, individuals from each egg-mass were divided into two groups. One group was fed on willow foliage and the other on box elder foliage. Foliage used to feed the larvae was collected from the same tree populations used to determine percentage parasitism. The foliage was disinfected to prevent disease (it was soaked for 15 min in a 0.25% solution of sodium hypochlorite) and thoroughly rinsed three times before use (Barbosa et al., 2000). Larvae were reared in 473 ml clear plastic cups. The development time for male and female O. leucostigma was recorded and represented the number of days from egg hatch to the emergence of adults. Adult wet mass was determined for unfed males and females after emergence using a Mettler AE 100 balance. Orgyia leucostigma wet mass has been found to correlate closely with female fecundity (Tammaru et al., 2002). The percentage parasitism of O. leucostigma on willow and box elder was calculated using our data from the rearing of O. leucostigma larvae collected from the same sites from which the egg masses parents were collected (Barbosa et al., 2001).
Differences in development time and mass of O. leucostigma feeding on box elder and willow were analyzed by ANOVA. Because the mass variances between males and females were very different, they were grouped to improve our statistical model (SAS, 1998). Diet (i.e., box elder or willow) and gender were considered fixed effects. Egg-masses from which larvae came (i.e., their family line) were considered as a random effect in the analysis.
Contingency tables were used to measure the association between parasitism and larval host tree species (SAS, 1998). A Pearson χ2 statistic was used for comparisons of observed and expected parasitism frequencies by the different parasitoid species and for comparisons of overall parasitism in box elder and willow.
The development of female O. leucostigma was significantly more rapid when the larvae were fed on willow foliage than when fed on box elder foliage (t = −3.7, d.f. = 124, P = 0.0014) (Figure 1). Female O. leucostigma were significantly heavier on willow than on box elder (t = 3.0, d.f. = 161, P = 0.0165) (Figure 2), indicating the greater suitability of willow for female O. leucostigma. No significant differences in development time (Figure 1) or mass (Figure 2) were observed among males. However, the sex ratio of larvae in both host plants was the same (1 : 1) and thus there was an overall difference in larval development time in each host plant species.
The slow-growth-high-mortality hypothesis would predict higher parasitism on the slower developing box elder fed larvae. However, the overall parasitism of O. leucostigma larvae was significantly higher on willow than on box elder (χ2 = 11.83; P<0.001) (Table 1), contradicting the prediction of the slow-growth-high-mortality hypothesis. Nevertheless, the parasitism of O. leucostigma by an undescribed Casinaria species was greater on box elder than on willow (85.7% parasitism on box elder vs. 14.3% on willow).
Table 1. Association between parasitism and host plant species for Orgyia leucostigma parasitoids in box elder and willow. Numbers represent overall percentage parasitism of all O. leucostigma larvae collected from 1991 to 1997. Absolute numbers of parasitoids are given in parentheses
Overall average percentage parasitism on
Total parasitism of O. leucostigma on box elder and willow was significantly different (χ2 = 11.83, P<0.001).
If we had merely considered parasitism by Casinaria spec. we would have concluded that the prediction of the slow-growth-high-mortality hypothesis was supported. Our findings suggest that different parasitoid species respond differently to the differential growth of O. leucostigma in box elder and willow. Overall however, the longer developmental time of O. leucostigma in box elder did not result in a greater parasitism compared to that of larvae on willow. Instead, parasitoids inflicted more mortality on O. leucostigma on willow than on box elder.
Differences in the levels of overall parasitism among larvae on box elder and willow were not likely to have been due to differences in host abundance on the two tree species. The total number of O. leucostigma larvae on box elder and willow over 7 years of field collections were not substantially different (a yearly average of 64 vs. 61.4 larvae on box elder and willow, respectively).
Because the parasitoids that attack O. leucostigma are polyphagous, another reason that could explain the larger proportion of parasitized larvae on willow might be differences in the number of other available potential host species on each tree. That is, a generalist parasitoid might be more attracted to, or forage longer in, trees that present more potential host species, particularly if they are also abundant hosts. Willow trees present more species of Lepidoptera than box elder trees in our system (71 macrolepidopteran species in willow and 61 macrolepidopteran species in box elder). However, Barbosa et al. (2001) reported that parasitism in box elder was generally twice that on willow in lepidopteran species other than O. leucostigma.Barbosa et al. (2001) considered the same generalist parasitoid species as in the present study, and their study was conducted in the same habitats and at the same time so it is unlikely that the higher parasitism levels in O. leucostigma found in willow was due to a higher Lepidoptera diversity on this tree.
Clancy & Price (1987) reported that bigger and faster developing sawflies were parasitized more than smaller, slowly growing sawflies. It has been observed that some parasitoids are often selective and prefer to oviposit on large hosts (Luck, 1990). Thus, fast developing insects that grow large perhaps represent a better quality resource for most parasitoids than smaller hosts. However, other parasitoid species prefer small hosts. The parasitoids that attacked O. leucostigma were mostly generalist species (with the exception of Cotesia delicata, Carcelaria amplexa, and Elacertus spec.) and included species that preferred small as well as large hosts.
Studies by Häggstrom & Larsson (1995) and Loader & Damman (1991) assessed whether herbivore development time affected the mortality imposed by a suite of natural enemies. To the best of our knowledge, these have been the only studies that have tested the slow-growth-high-mortality hypothesis on a free-feeding insect by evaluating the impact of various species in a natural enemy community. However, Häggström & Larsson (1995) only looked at predation and Loader & Damman (1991) only considered parasitism by species small enough to fit through the 1.4 mm mesh used to cage their plants, and thus may have not evaluated all the parasitoids of Pieris rapae. The present study is the first to test the slow-growth-high-mortality hypothesis in the field, considering an entire parasitoid assemblage attacking a free-feeding herbivore, and although correlational, it represents the long-term (7 years) outcome of the interactions between O. leucostigma and its parasitoids. Benrey & Denno (1997) and this study are the only ones to have tested the slow-growth-high-mortality hypothesis on herbivores feeding on distantly related plants. Their study focused on one parasitoid species, ours focused on a parasitoid assemblage. Both studies failed to support the hypothesis.
Lill & Marquis (2001), who focused on an endophytic herbivore, and this study, are the only ones to have tested the slow-growth-high-mortality hypothesis focusing on the parasitoid community attacking an herbivore species. Lill & Marquis (2001) analyzed the effect of the parasitoid community attacking a leaf-tying herbivore on the same plant species, whereas our study analyzed the effect of the parasitoid community on a free-feeding herbivore feeding on two different host plant species. Both studies failed to support the slow-growth-high-mortality hypothesis. So far the slow-growth-high mortality hypothesis appears to hold in interactions between free-feeding herbivores and their predators or parasitoids only when tested on the same or closely related plant species.
We acknowledge Astrid Caldas and Mary Christman for their support with the statistical analyses, Holliday Obrecht (Patuxent Wildlife Research Center) for his logistic assistance, and Ignacio Castellanos for his helpful comments. This Research was supported in part by Maryland Agricultural Experiment Station Project MD-H-201.