Hydrobiologia 482: 191–196, 2002. © 2002 Kluwer Academic Publishers. Printed in the Netherlands.
191
Novel observations of midge and mosquito larval population dynamics in leaves of the northern pitcher plant, Sarracenia purpurea L. Robert Hamilton IV1 & Richard M. Duffield∗ Department of Biology, Howard University, Washington, DC 20059, U.S.A. Tel.: +1-202-806-6127. Fax: +1-202-806-4564. E-mail:
[email protected] (1 Author for correspondence) Received 5 June 2002; accepted 12 July 2002
Key words: Metriocnemus knabi Coq., Wyeomyia smithii (Coq.), midge, mosquito, diptera larvae, Sarracenia purpurea L., population dynamics, phytotelmata
Abstract The invertebrate communities in Sarracenia purpurea were characterized by surveying the contents of 474 leaves from six pitcher plant populations in the eastern United States. More than 8200 invertebrate specimens, both living and dead, were recovered. Midge and mosquito larvae comprised 7907 (96%) of the specimens, with a mean of 16.9 dipteran larvae per leaf. Although midge larvae were present at all collection sites, mosquito larvae were absent from two of the sites. In the latter sites, the number of midge larvae per leaf was greater. This report documents for the first time that there is no statistical difference between the average number of Diptera larvae per leaf for sites that contain both midge and mosquito larvae compared to sites that contain only midge larvae. It appears that pitcher plants maintain an average number of larvae per leaf based on a number of interacting factors which we do not fully understand. This investigation documents that in the absence of mosquito larvae, more midge larvae are found per leaf per leaf than would be predicted based on data from sites that contain both larval taxa.
Introduction The northern pitcher plant, Sarracenia purpurea L., is distributed in the eastern United States, primarily in bogs, fens and other habitats with wet, infertile soils. The fluid-filled leaves of this carnivorous species attract prey by a combination of leaf shape, leaf coloration, extrafloral nectar release and other olfactory cues (Juniper et al., 1989). Some of the insects that are attracted to the leaves fall in and drown. Besides acting as insect traps, the leaves also provide habitat for a wide variety of insects, other arthropods, and microorganisms. Documented inhabitants include aquatic mites, several different groups of crustaceans including copepods (Hamilton, 2000), amphipods, isopods and cladocerans, bacteria (Istock et al., 1975; Prankevicius & Cameron, 1991), protozoans ∗ Present address: Graduate Program in Ecology and Evolution,
Rutgers University, New Brunswick, NJ 08901, U.S.A.
(Addicott, 1974), rotifers, nematodes and immature insects (Fish & Hall, 1978; Rymal & Folkerts, 1982; Heard, 1994a; Harvey & Miller, 1996; Hamilton et al., 1996; Hamilton et al., 1998). These invertebrates can be classified as regular inhabitants (inquilines), prey, occasional associates, or plant herbivores, depending on the nature and extent of their interactions with S. purpurea (Rymal & Folkerts, 1982). The regular inhabitants, or inquilines, are obligate inhabitants of S. purpurea. They complete either their entire life cycle or only immature stages within the leaves. These inquilines include mites (Fashing & O’Connor, 1984), copepods (Hamilton et al., 2000), rotifers (Bateman, 1987; Petersen et al., 1997) and larvae of three dipteran species. The three dipteran species are the midge, Metriocnemus knabi (Coq.) (Chironomidae), the mosquito, Wyeomyia smithii (Coq.) (Culicidae), and the sarcophagid fly, Fletcherimyia (Blaesoxipha) fletcheri (Aldrich) (Sarcophagidae) (Rymal & Folkerts, 1982).
192 The dipteran inquilines are present in different quantities and at different times of the year. When present, there is generally only one B. fletcheri larva per leaf (Forsyth & Robertson, 1975). In contrast, the midge and mosquito larvae, when present, can be very numerous. The midge and mosquito larvae are among the most frequently studied inhabitants of S. purpurea, in part because they are usually the dominant macroinvertebrates living in the pitcher plant leaves (Harvey & Miller, 1996). Furthermore, both species are easily reared in the laboratory, which facilitates experimental manipulation under controlled conditions (Bradshaw, 1983; Heard, 1994a). The larvae of all three dipterans species feed on organic matter derived from the decomposition of captured prey. Fletcherimyia larvae are considerably larger than those of the mature midge or mosquito and feed on prey items floating on the surface of the leaf water (Addicott, 1974; Bradshaw, 1983). Wyeomyia smithii larvae are found actively swimming in the water column, filter feeding on both microorganisms and particles produced by the decomposition of prey items (Addicott, 1974; Heard, 1994a). The midge larvae are found in the bottom of the cone-shaped leaves where they feed on prey by tearing them apart (Bradshaw & Creelman, 1984). While the midge larvae eliminate some potential food for Wyeomyia, they also accelerate resource processing (Buffington, 1970; Bradshaw, 1983). Each of the dipteran inquilines feeds at different strata in the leaves and exhibits different feeding strategies. Literature reports that the three species partition the leaf spatially and temporally (Fish & Hall, 1978; Bradshaw & Creelman, 1984; Heard, 1994a). Resource partitioning in these leaves depends upon the numbers and kinds of inhabitants, the age of the leaf and the amount of non-living organic matter in the leaf (Fish & Hall, 1978). The goal of this investigation was to compare the composition of the invertebrate communities associated with pitcher plant leaves across a wide geographic range. It was unknown to us at the time that the leaf samples were collected, that two of the sites did not contain mosquitoes. It was not until later in the study that we realized that these sites could provide a unique opportunity to gain insight into the population dynamics between midge and mosquito larvae in a natural setting. When data on invertebrates associated with S. purpurea populations was analyzed, it became evident that pitcher plants sites could be separated into two classes based on the types of Diptera larvae present.
The first set of sites and typical of most sites we encountered, consist of pitcher plants that contain both midge and mosquito larvae in the leaves. However, we also encountered several pitcher plant sites where plants harbor midge larvae but no mosquito larvae.
Methods Collection sites The Sarracenia purpurea collection sites were located in Maryland, Pennsylvania, West Virginia, North Carolina, and Georgia. The sites included Big Run Bog, Tucker County, West Virginia; Christner Bog, Somerset County, Pennsylvania; Nassawango Creek Site, Wicomico County, Maryland; Suitland Bog, Prince Georges County, Maryland; Lumber River Site, Robeson County, North Carolina and New Hope Bog, Tattnall County, Georgia. The Suitland Bog and Nassawango Creek Site pitcher populations are natural; Big Run Bog and Christner Bog populations are transplanted; and the source of Lumber River Site and New Hope Bog populations is unknown. Sample collection Samples were collected between 11 March 1996 and 22 November 1997. Samples were collected from mature leaves. No more than two leaves were sampled from the same rosette. The volumes of each individual leaf were not measured. At all sites except Big Run Bog, pitcher plants were left intact. The fluid contents in each leaf was stirred with a small tapered spatula to re-suspend debris and organisms, then the liquid and debris were withdrawn from each leaf using a pipette (0.4 cm I.D.) with rubber bulb according to the method used by Hamilton et al. (2000). At Big Run Bog, several plants were scooped out by hand, placed in large plastic pans and transported back to the laboratory. Each leaf was then cut at the base and removed from the plant. The liquid contents of each leaf were poured into a 50-ml conical centrifuge tube and the water was decanted. The remaining liquid and debris were preserved in 70% ethanol. Sample analysis Each sample was observed under a dissecting microscope. The number of midge and mosquito larvae were counted and recorded. Other insects were identified to order and family. Macroinvertebrate taxa other than
193 insects were identified to class and order when possible. A few specimens were too severely degraded to be identified ( 0.05) between sites that harbored both species (Suitland and Nassawango) and those that did not (Christner and Big Run) and had similar leaf sample sizes (Table 2b, Fig. 1).
Discussion This investigation compared the average number of Diptera larvae per mature leaf at pitcher plant sites that contain both midge and mosquito larvae compared to sites whose plants contain only midge larvae. Analysis of our collection data indicates that the average number of Diptera larvae per leaf is not statistically different whether the sites contain midge and mosquito larvae or contain only midge larvae. In the absence of Wyeomyia smithii larvae, the average number of midge larvae (Metriocnemus knabi) per leaf increases. We did not observe any sites that contained mosquito larvae without midge larvae. ANOVA analyses demonstrated that there was no statistical difference between the average numbers of Diptera per leaf in
sites that contain both species versus sites that contain only the midge. Samples from the six collection sites contained a total of two sarcophagid larvae. They were not common organisms in our samples or at our collection sites. The absence of sarcophagids is surprising because they are a commonly reported inquiline. Harvey and Miller (1996) and Rango (1999) reported highest densities in natural pitcher plant populations in late July or early August. Hardwick and Giberson (1996) reported highest densities in both natural and transplanted pitcher plant populations in August. We made multiple collections during each month from April to October, so it is unlikely that the sarcphagids were present, yet the sampling regime missed them. Since so few sarcophagids were present, their influence on the collection data is minimal if any. The dominant macroinvertebrates in our samples were midges and mosquitoes. This is a commonly reported occurrence (Fish & Hall, 1978; Rymal & Folkerts, 1982; Bradshaw 1983; Heard 1994a; Hardwick & Giberson, 1996; Harvey & Miller, 1996; Hamilton et al., 1998; Rango, 1999). Despite being found in nearly equal total numbers, mosquitoes were completely absent from two populations. One explanation for the absence of mosquitoes is that they were never able to colonize these two sites in which they were absent from. Big Run Bog, WV and Christner Bog, PA are transplanted pitcher plant sites. Records for the introduction of S. purpurea at Christner Bog (estimated to contain between 500 and 1000 plants) and Big Run Bog (estimated to contain between 6000 and 10 000 plants are known, and each is over 40 years old. These obviously thriving populations, although transplanted, provided a unique opportunity for comparison to data from natural pitcher plant populations. Yet, despite their age and size it is possible that W. smythii never got established at these sites. Istock et al. (1983) and Heard (1994b) both reported that W. smithii is a poor flier. It may not be able to travel far enough to colonize some transplanted pitcher plant populations. Hardwick & Giberson (1996) reported a lower abundance of W. smithii in transplanted populations that were relatively close to natural populations. Another possibility is that one or more other organisms prevented mosquito colonization at Big Run Bog and Christner Bog. While the midge and mosquito have been studied extensively, there are a variety of other organisms living in the pitcher plant leaves that may directly or indirectly affect the population
194 Table 1. Mean number of Diptera larvae collected from leaves of Sarracenia purpurea at six different collection sites Site
Leaves sampled
Total midges
Total mosquitoes
Total flesh flies
Total Diptera
Mean no. of Diptera/ leaf
Standard deviation
Christner Bog, PA Big Run Bog, WV Suitland Bog, MD Nassawango Creek, MD Lumber River, NC New Hope Bog, GA
110 139 93 112 9 11
1943 2424 800 810 63 59
0 0 848 755 99 106
1 1 0 0 0 0
1943 2424 1648 1565 162 165
17.7 17.4 17.7 14.0 18.0 15.0
12.4 12.2 10.1 9.1 8.2 6.4
Totals
474
6099
1808
2
7909
Table 2. ANOVA comparing total numbers of Diptera at sites with only midges and sites with midges and mosquitoes. There is no significant difference in total number of Diptera (F value 2.03 < F critical value 3.86) (a), but highly significant difference (F value 71.69 >>> F critical 3.86) in numbers of midges at sites with only midges and sites with midges and mosquitoes Source of Variation
SS
df
MS
F
P value
(a) ANOVA for total numbers of Diptera at sites with only midges and sites with midges and mosquitoes. Between Groups 378.25 1 378.25 2.038 0.154 Within Groups 94832.89 511 185.58
(b) ANOVA for total numbers of midges at sites with only midges and sites with midges and mosquitoes. Between Groups 9345.28 1 9345.28 71.69 2.687E-16 Within Groups 66613.84 511 130.36
F crit
3.86
3.86
Figure 1. Midge and mosquito larvae densities in Sarracenia purpurea leaves: ±1 Standard Error. Sites: Christner Bog (CB), Somerset Co., PA; Big Run Bog (BRB), Tucker Co., WV; Suitland Bog (SB), Prince Georges Co., MD; Nassawango Creek Site (NCS), Wicomico Co., MD; Lumber River Site (LRS), Robeson Co., NC; New Hope Bog (NHB), Tattnall Co., GA.
dynamics of the midge and mosquito larvae (Petersen et al., 1997; Hamilton et al., 2000). Olfactory cues or metabolic products from other organisms may inhibit ovipositing females from laying eggs. We have only a
limited understanding of the community dynamics of the assemblages of organisms inhabiting S. purpurea leaves.
195 It is also possible that some physical or chemical condition specific to just these two sites prevented mosquito colonization. However, the chemical composition of the leaf fluid and surrounding water was not analyzed. Therefore, further analysis is necessary to confirm or refute this possibility. Regardless of why there were no mosquitoes at these two sites, it appears that the midge larval populations increased in the absence of mosquito larvae. Both larvae feed upon a shared food resource, so one could influence the other. In natural settings, it does not appear that the absence of the mosquito larvae negatively affect the number of midge larvae, since species may overlap in resource use without being resource limited if the shared resource is not in short supply (Morin, 1999). Whether or not food is the limiting resource, the data suggest that the midge larvae are able to convert the food resources into additional recruitment, therefore increasing population density in the absence of mosquito larvae. Pitcher plant leaves, like every habitat, have a specific carrying capacity. We suggest that the carrying capacity of the leaf is based in part on the volume of the leaf. Each can support a maximum number of inhabitants based on a variety of factors including leaf volume, species composition, and the number of individuals present. In the case of the two larval dipteran inhabitants studied in this investigation, there was no significant difference in the mean number of Diptera larvae per leaf among sites that contained both midges and mosquitoes versus sites containing midges only. In the absence of mosquito larvae in the leaves, the number of midge larvae increase to near the carrying capacity of the S. purpurea leaf. It is possible that the midge larvae could respond to the absence of the mosquito by increasing the size per individual rather than number of individuals. Although possible, this scenario is not what we observed. In our investigation, like Rango (1999), the natural S. purpurea populations contained both inquilines although each individual leaf did not necessarily have both. This investigation demonstrates that at least in transplanted populations of S. purpurea the mean number of larval Metriocnemus knabi per leaf is elevated in the absence of Wyeomyia smithii.
Acknowledgements We thank the following organizations and people for help with this project. USDA-Forest Service (East-
ern Region) for partial support during this project. R. Hamilton IV was supported in part by a fellowship from a National Science Foundation Traineeship in Plant Biology (GER 9354916). We thank Doug Sampson, MD/DC Nature Conservancy for allowing access to the Nassawango Creek Site and the Maryland-National Capital Park and Planning Commission for allowing access to Suitland Bog, MD. We thank Mary McKenna, George Middendorf, and Emilie Stander for their comments during the development of the manuscript. RHIV thanks Colleen Hatfield, Peter Smouse, and Peter Kourtev for their help with the statistical analyses. Voucher specimens are held in the Department of Biology, Howard University, Washington, DC (RMD). References Addicott, J. F., 1974. Predation and prey communities structure: an experimental study of the effect of mosquito larvae on the protozoan communities of pitcher plants. Ecology 55: 475–492. Bateman, L. E., 1987. A bdelloid rotifer living as an inquiline in leaves of the pitcher plant, Sarracenia purpurea. Hydrobiologia 147: 129–133. Bradshaw, W. E., 1983. Interaction between the mosquito Wyeomyia smithii, and the midge Metriocnemus knabi, and their carnivorous host, Sarracenia purpurea. In: Frank, J. H. & L. P. Lounibos (eds), Phytotelmata: Terrestrial Plants as Hosts for Aquatic Insect Communities. Plexus, Medford, NJ: 161–189. Bradshaw, W. E. & R. A. Creelman, 1984. Mutualism between the carnivorous purple pitcher plant and its inhabitants. Am. Midl. Nat. 11: 294–303. Buffington, J. D., 1970. Ecological considerations of the cohabitation of pitcher plants by Wyeomyia smithii and Metricnemus knabi. Mosquito News 30: 89–90. Fashing, N. J. & B. M. O’Connor, 1984. Sarraceniopus – a new genus for histiostomatid mites inhabiting the pitchers of the Sarraceniaceae (Astigmata: Histiostomatidae). Int. J. Acarol. 10: 217–227. Fish, D. & D. W. Hall, 1978. Succession and stratification of aquatic insects inhabiting the leaves of the insectivorous pitcher plant, Sarracenia purpurea. Am. Midl. Nat. 99: 172–183. Forsyth, A. B. & R. J. Robertson, 1975. K reproductive strategy and larval behavior of the pitcher plant sarcophagid fly, Blaesoxipha fletcheri. Can. J. Zool. 53: 174–179. Hamilton, R. IV, 1998. Macro- and microinvertebrates associated with the purple pitcher plant, Sarracenia purpurea L. M. S. Thesis. Howard University, Washington, DC: 127 pp. Hamilton, R. IV, M. Whitaker, T. C. Farmer, A. A. Benn & R. M. Duffield, 1996. A report of Chauliodes (Megaloptera:Corydalidae) in the purple pitcher plant, Sarracenia purpurea L. (Sarraceniaceae). J. Kansas Entomol. Soc. 69: 257–259. Hamilton, R. IV, R. L. Petersen & R. M. Duffield, 1998. An unusual occurrence of caddisflies (Trichoptera:Phryganeidae) in a Pennsylvania population of the purple pitcher plant, Sarracenia purpurea. Ent. News 109: 36–37. Hamilton, R. IV, J. Reid & R. M. Duffield, 2000. Rare copepod, Paracyclops canadensis (Willey) common in leaves of Sarracenia purpurea L. Northeastern Nat. 7: 17–24.
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