ABSTRACT

Native ecosystems are changing rapidly by the invasion of species, many of which thrive in their new environments because of lack of predators. If predators present in the new location of the invasive attack the invasive, it may be controlled, preventing a population explosion. I studied an infestation of plume moth (Platyptilia carduidactyla) larvae in two species of thistle, one invasive and one native. I also performed experiments to examine larval choice of thistle flowers and consumption of seeds. Samples were collected from Reese's Swamp, Cheboygan County, Michigan. Flowers were opened to determine infestation, and larva were taken to use for the choice experiments. There was no difference in the cumulative infestations of the native thistle Cirsium muticum and the invasive species C. palustre. However, more individual C. palustre than C. muticum plants were infested. Among only the infested plants, C. muticum had a higher average infestation. These results are probably artifacts of physical plant structure, such as flower density. They cannot be accurately interpreted without information on relative thistle densities in Reese's Swamp. The results of the choice experiments were also inconclusive, because of possible larval bias from their host plant origin. There was no significant difference in larval choice of thistle flowers. Statistically more seeds of C. palustre were consumed. The question of plume moth preference for species of thistle cannot be answered without further research, yet we can draw encouraging general conclusions about the state of thistles in Northern Michigan. The herbivory demonstrated in my study is a hopeful assurance that invasive thistles will not cause the extinction of native species of thistle.

INTRODUCTION

            Native ecosystems are changing rapidly by the invasion of species, many of which thrive in their new environments. The study and control of invasive species is important to ecologists and conservation biologists, as well as anyone who would like to preserve the pristinity of nature. Biological invaders can alter community structures and population dynamics of native ecosystems (Elton 1958, Mooney and Drake 1986) as well as their ecosystem level processes, such as water and energy cycling (Ramakrishnan and Vitousek 1989). Invasion by species is a very natural process, forming the basis for species distribution (Elton 1958). However, the normally slow spread of organisms has been drastically accelerated in recent years because of increased human movement (eg Heywood 1989). Clearly, it is our duty to both prevent excessive invasion due to our interference, and to control invasive species that we have propagated. Otherwise, irreplaceable ecosystems may be altered forever, causing the loss of important information about the world.

            While some invasive species experience a population explosion when brought to totally new areas, many begin a slow, steady growth (Elton 1958). Invasive species, when not hindered by abiotic factors, frequently lack the biotic limitations that keep them in check in their native localities. Introduced reindeer on South Georgia island and introduced rabbits in Australia both rapidly filled their new habitats (Krebs 1994). Some organisms are simply well adapted to propagating in new areas (Kareiva et al. 1993). These pioneer species have high fecundity and short generation times, and can be different species of a genus already present in the new location. The same predators or herbivores that prey on the native species will also keep the new species in check, preventing a population explosion (eg rodents on invasive seedlings, Ostfeld et al. 1997). However, invading species may be more resistant to herbivory, giving them an advantage over natives. A more fit invasive may slowly crowd out native species.

            Cirsium palustre (L.) Scop. is a European species of thistle (Asteraceae) that appears better defended against herbivory than its North American counterparts. It has sharp, dangerous leaves and is exceedingly spiny, especially compared to the native Northern Michigan swamp thistle C. muticum Michaux (Voss 1996). C. palustre was first collected in the Upper Peninsula of Michigan by Fernald in 1935 (Fernald 1950), but was found in the Lower Peninsula by Fernald in 1959 and is slowly making its way south (Voss 1996). Colonies of C. palustre are evident along roadside ditches and adjacent swamps. These unstable habitats are very vulnerable to invaders (Mooney and Drake 1986) and human movement is helping the plant to spread (Voss 1996). The relationship between C. palustre and C. muticum is not clear. While C. muticum, with its larger flowers and relatively unarmed stem, appears more attractive to herbivores than C. palustre, no comparative density data between the two species has been recorded. We do not yet know if C. palustre is crowding out its native counterpart, or if the two will continue to coexist. If C. palustre has a destructive effect on C. muticum, it may also harm the endangered sand dune thistle C. pitcheri (Torr.) Torrey & Gray.

            The artichoke plume moth Platyptilia carduidactyla (Riley) (Lepidoptera: Pterophoridae) (Neuzig 1987) is a seed predator that has been documented to prey on Cirsium species in California (Turner et al. 1987). I observed moth larvae in flower heads of both C. palustre and C. muticum in the cedar swamps around Pellston, Michigan. Although oviposition patterns of this plume moth are not known, the larva matures inside the flower head and eats the ovules of the flower. Mature flowers that have been host to a larva are missing most or all of their seeds and are filled with black frass. The exact ramifications of this herbivory on the total plant health and reproduction are not known; however, the destruction of infested flower heads is evident. The moth appears to be a generalist, not specialized to any one species of thistle, but may prefer species because of defense, plant size, or any number of other factors. I collected specimens of the two species of swamp thistle in order to analyze the preference of ovipositing plume moths. I also performed choice experiments using P. carduidactyla larvae to study larval preference of thistle flowers and seeds. Adult preference will guide inferences about possible differential herbivory on species of thistle in Northern Michigan. Larval preference may provide information about adult preference and about destruction of thistle flowers. I hypothesize that, because of lesser physical defenses and larger flowers, C. muticum will be preferred over C. palustre by P. carduidactyla.

METHODS

            Plants were collected from Reese's Swamp, Cheboygan County, MI (45o33'N; 84o41'W; T36N, R3W, S3) on July 17, 1998. Every seventh Cirsium palustre plant and every tenth C. muticum plant was sampled. However, since C. palustre was more mature than C. muticum, I skipped the plants that had already seeded. Great care was taken to avoid dramatic impact on C. muticum. I only collected the top flower cluster of the inflorescence of each plant to leave flowers for the reproduction of the plant. Thirty eight C. palustre and forty C. muticum plants were collected. Each flower was opened to identify infestation with Platyptilia carduidactyla larva. Infested flowers were hollowed out and had distinctive black frass inside, and most contained a larva. The larvae were saved for choice experiments. In total, 869 Cirsium palustre and 189 C. muticum flowers were sampled.

            Two choice experiments were performed with the larvae. For each replicate, one mature larva was placed in a dry petri dish and starved for 10 h. The replicates were kept at room temperature for the duration of the experiments. To test flower preference, a mature uninfested flower of each species was cut in half and placed an equal distance from the larva in each replicate (n = 16). Replicates were left for 26 h, after which the position of the larva was recorded. Larvae were found feeding on one flower head in all cases. To test seed preference and consumption, ten mature seeds of each species of thistle were placed an equal distance from the starved larvae in each replicate (n = 10). After a feeding period of 26 h, the number and type of consumed seeds were recorded.

            Statistical analyses were done with SYSTAT 5.2 (Wilkinson 1992) and by hand. Initially, chi squared analysis was performed to check for difference in the infestations (number of infested flowers per plant over total number of flowers per plant) of all samples of the two species of thistle. When no significant difference was found, I used chi squared analysis to check for differences in the distributions of infested plants (at least one infested flower = infested plant). Both chi squared analysis and an independent student's t-test were used to analyze the infestations of only the infested plants. The t-test was performed on the arcsine transform (arcsine ˆx) of the infestations. The great disimilarity between numbers of flowers per plants of the two species spurred an additional Mann Whitney-U test. This test checked for difference between the numbers of infested flowers on each plant. Chi squared analysis was used to check for differences in head choice and in the distribution of thistle seeds consumed.

RESULTS

            Chi squared analysis of the 78 total plants and the 1058 total flowers showed that there was no difference in the cumulative infestations of the plants (number of infested flowers / total number of flowers for all plants, X2 = 1.97, df = 1, Table 1). However, more of the Cirsium palustre plants were infested than C. muticum (X2 = 16.78, df = 1, Table 1). In a comparison between only the infested plants (29 C. palustre and 12 C. muticum), C. muticum plants were statistically more infested than C. palustre (t = -4.617, df = 39, p < 0.05, Table 1). Chi squared analysis of the 962 flowers of these infested plants confirmed the statistical difference (X2 = 13.18, df = 1, p < 0.05). There were more actual infested flowers per plant of C. palustre than C. muticum.(n = 40, U = 266.5, p < 0.05). There was no statistical difference in the larvae choice between thistle flowers (n = 16, X2 = 1, df = 1), but the larvae consumed more seeds of C. muticum than C. plaustre (n = 10, X2 = 22.04, df = 1, p < 0.05).

DISCUSSION

            My statistical analysis showed that the overall infestations of Cirsium palustre and C. muticum were the same. Despite the physical defenses and smaller flowers of C. palustre, ovipositing plume moths did not avoid them entirely in favor of C. muticum. Platyptilia carduidactyla appears to be a general enough ovipositor to use many species of thistle as hosts. Turner et al. (1987) successfully reared the plume moths in 15 Cirsium species, as well as several other members of the Asteraceae family. While they did not include the relative successes of the moths hosted in their respective species, the moths did survive in naturalized as well as native plants. My discovery of P. caruidactyla in both a native as well as an invasive species is a good extrapolation of their work.

            Selective analysis of the infestation data provides additional interesting information. Plume moths oviposited in more Cirsium palustre than C. muticum plants (76% of plants versus 30%, respectively), but infested C. muticum plants had higher average infestations than infested C. muticum plants (43% <±> 17 versus 16% <±> 4, respectively). Unfortunately, comparative infestation studies are scarce in most cases, and are almost nonexistent for plants without agricultural use such as the Asteraceae. Also, without density data on the two species of Northern Michigan thistle, many infestation comparisons become meaningless. A greater density of C. palustre in Reese's swamp would explain the greater number of infested C. palustre plants. In this case, ovipositing plume moths expressed no preference for C. palustre, the results were an artifact of plant density. On the other hand, if C. muticum has a higher density, or if both species are present to the same degree in Reese's Swamp, there was a preference for C. palustre. This preference could be explained by the greater number of flowers on C. palustre stalks, depending on moth criteria for oviposition. Insects are known to choose oviposition sites by visual stimuli (eg Kennedy 1976), as well as olfactorial (eg La Berre and Launois-Luong 1976) and various other characteristics (eg Saringer 1976, Courtney and Kibota 1990) of host plants. Each insect species must be studied to determine specific preference. C. palustre flowers are also smaller than C. muticum flowers, and this may be better for Platyptilia carduidactyla in some way.

            The differences in infestations of infested plants was probably an artifact of the different total numbers of flowers per plants of the two species. While infested Cirsium muticum plants had statistically higher infestations, they also have fewer flowers per plant. Explanation of these results depends of the oviposition behavior of the moths. If Platyptilia carduidactyla tends to oviposit in a certain proportion of flowers per host plant, then that proportion is greater in C. muticum. However, if the moth leaves an empirical number of eggs in each host plant, more eggs are left in C. palustre plants. Both of these oviposition patterns have been documented for different species of insects, but studies of the plume moth Platyptilia carduidactyla have not been conducted.

            Platyptilia carduidactyla showed no preference for flower heads in my experiment. This has very little relevance to adult plume moth oviposition preference. I theorized that larval choice would indicate the better flower material for larval survival, and that adults would also choose the better food for their larvae. Of course, this theory has not been proven. In addition, lepidopterous larvae tend to exhibit preference in choice tests based on the host plant they were raised in (Hanson 1976). I did not regulate or record the origin of the test larvae, and this probably skewed my results. The seed consumption experiment is slightly more enlightening. P. carduidactyla larvae consumed more Cirsium muticum seeds than C. palustre seeds. This implies that larvae will do more damage to C. muticum. Once again, this test is biased because of the origin of the P. carduidactyla larvae. Also, infested flowers tended to be totally destroyed at maturity; the rate of their consumption is irrelevant. However, P. carduidactyla larvae have been observed to bore through stems to new flowers in search of additional food. A higher consumption rate would mean greater damage to thistles, especially for C. palustre with its smaller flowers. A no choice experiment (eg Butter et al. 1997) would be a much better indicator of the consumption rate of larvae.

            The question of plume moth preference for species of thistle cannot be answered without further research. My study was hampered by lack of literary background and experimental precedence. In addition to elementary research on plume moth natural history, a census of thistle densities and growth patterns would be especially helpful. Slightly poor experimental design prevents any specific conclusions about moth preference, yet we can draw encouraging general conclusions about the state of thistles in Northern Michigan. Although the invasive Cirsium palustre is making its way south, it is moving slowly. Judging from my superficial field observations, C. palustre is not crowding out C. muticum to any extreme extent. Both species were successfully sharing habitat space, and there was no evidence of C. palustre population explosion. The reason for this can be taken from my research. The native plume moth Platyptilia carduidactyla is attacking the invasive European C. palustre. This herbivory is a hopeful assurance that invasive thistles will not cause the extinction of native species of thistle. While the new thistles are an eyesore (Voss 1996), perhaps they will be a continual reminder of the effects of human interference on ecosystems and the dangers of invasive species.