Table of Contents:
Keywords: acid rain, assembly rules, bogs, indicator species, nitrogen deposition, Sarracenia purpurea, wetlands |
|
Carnivorous plants are curiosities of the plant kingdom that have fascinated naturalists, botanists, and ecologists for centuries. Before the mid-1800s, scientists were reluctant to accept that plants could consume insects and other small invertebrates, but with a series of elegant experiments, Darwin (1875) provided conclusive evidence for carnivory by the common English sundew. By the end of the 20th century, nearly 600 species of carnivorous plants had been identified and described (see Ellison & Gotelli 2001 for a review on current research on carnivorous plants around the world). Carnivorous plants have evolved primarily in nutrient-poor, high-light environments. Peatlands (bogs, seepage swamps, and fens) are the most common habitat in which to find these plants, but they also grow on high-elevation massifs such as sandstone tepuis in Venezuela and Guiana (Givnish et al. 1984) and granitic inselbergs in Africa (Dörrstock et al. 1996, Seine et al. 1996).
Since 1997, my colleagues Nicholas Gotelli (University of Vermont) and Leszek Bledzki (Mount Holyoke College) and I have been studying the ecology and biological diversity of pitcher-plant bogs in Massachusetts and Vermont. The initial focus of our research was on the interactions between the carnivorous pitcher plant (Sarracenia purpurea L.) and the community of invertebrates that live in the rainwater that accumulates in the pitchers. In the last few years we have expanded our work to include inventories of ants and rotifers in bogs, and the effects of nitrogen deposition (one component of "acid rain") on the pitcher-plant microecosystem. Along with our colleagues throughout the world, we have been developing the Sarracenia system as a model for understanding population dynamics, community structure, and ecosystem processes (Ellison et al. 2002). Here, I highlight some of our key results that suggest strongly that Sarracenia purpurea and its associated aquatic ecosystem is an indicator of nitrogen deposition rates and I discuss the long-term impacts of nitrogen deposition on populations of pitcher plants and the surrounding peatlands.
Peatlands are waterlogged wetland ecosystems in which the extremely slow rate of decomposition results in the accumulation of dead plant matter ("peat"). Although they only occupy 3-7% of the Earth's land area, the peat in peatlands accounts for nearly one-third of the global pool of soil-bound carbon (Gorham 1991). Because most peatlands occur in high (northern) latitudes where global temperature rises are expected to be greatest (IPCC 2001), there is a great deal of research focused on whether global warming will result in an acceleration of decomposition rates in peatlands and a release (primarily as methane) of the carbon stored in peatland soils (e.g., Bubier & Moore 1994, Bubier et al. 1998).
"Pitcher plants" refer to carnivorous plants of three unrelated plant families, Sarraceniaceae, Nepenthaceae, Cephalotaceae, whose leaves (in plants of the Sarraceniaceae) or tendrils (in plants of the Nepenthaceae and Cephalotaceae) have been modified into pitfall traps that capture and digest animal prey. The 87 species of Nepenthes (the only genus in the family Nepenthaceae) occur from Palau and Australia westward through southeast Asia and into Madagascar, and the one species of Cephalotus (Cephalotaceae) is found only in southwestern Australia. The family Sarraceniaceae grows only in the western hemisphere, and is composed of three genera: Heliamphora (six species) which grows on tepuis; Darlingtonia (one species), which grows in serpentine seepage fens in southern Oregon and California; and Sarracenia (10 species), which grows in bogs, fens, and seepage swamps of the eastern United States and throughout Canada. All species of Nepenthes and the nine species of Sarracenia that occur in the southeastern United States digest prey directly with plant-secreted proteolytic enzymes (Heslop-Harrison 1978). Sarracenia purpurea (illustrated in the photograph at the top of this article), the focus of our research, depends on a community of bacteria, protozoa, and fly larvae to break down the captured prey and release the nutrients to the plant (Fish & Hall 1978). See pitcher-plant community.
Sarracenia purpurea is a long-lived (> 50 yr), rosette-forming perennial plant. We study the northern subspecies of S. purpurea, S. purpurea ssp. purpurea (Raf.) Wherry, which is one of the most characteristic plants of ombrotrophic ("rain fed") bogs throughout Canada and the eastern United States from Maine southward to northern Maryland (Gleason & Cronquist 1991). Individual plants collect rainwater in their pitcher-shaped leaves, and prey are attracted to the extrafloral nectaries on the lip of the brightly-colored pitchers. These prey occasionally fall into the pitchers and subsequently drown, but the northern pitcher plant is not a very efficient predator (Newell & Nastase 1998). Most prey that wander in to the pitchers subsequently wander out; on average fewer than 1% of the insects that enter a pitcher actually are captured, and each pitcher catches approximately 1 prey item (usually an ant or a fly) every other day during the growing season (Newell & Nastase 1998). When it flowers, S. purpurea produces one single-flowered inflorescence. The flower bud is set at the end of the previous growing season (Shreve 1906), and floral development recommences after a winter dormancy. Voles, deer, and larvae of moths (Exyra fax Grote) eat the buds, flowers, and later, fruit. Bumble bees (Bombus spp.) and the adults of the sarcophagid fly Fletcherimyia fletcheri (Aldrich), whose larvae also inhabit the pitchers, pollinate the large, umbrella-shaped flowers (Burr 1979). Capsules mature by late September, and seeds disperse passively by wind and water throughout the winter (Ellison & Parker 2002). The seeds germinate readily following a single season of winter dormancy (Ellison 2001), but they do not appear to persist in the seed bank (unpublished data of A. M. Ellison & H. R. Steinhoff).
The remarkable community of bacteria, protozoa, and animals that inhabits the rainwater-filled pitchers of Sarracenia purpurea has been the subject of numerous ecological investigations (see reviews in Fish & Hall 1978 and Ellison et al. 2002). Prey captured by the plant, (such as the ant Tapinoma sessile, are first chewed and shredded by slime mites (Sarraceniopus gibsoni Fashing & O'Connor) and midge larvae (Metriocnemus knabi Coq.). The fragments that remain are colonized by bacteria, which continue the decomposition process. The bacteria are eaten in turn by rotifers (Habrotrocha rosa Donner) and mosquito larvae (Wyeomyia smithii (Coq.)), which themselves are eaten by the top predator in the system, the solitary and cannibalistic larvae of the fleshfly Fletcherimyia fletcheri.
Many of these species are found only in association with pitcher plants. For example, each species of Sarracenia, Darlingtonia, and Heliamphora appears to have a unique species of slime mite that lives only in its host's leaves (this example of coevolution is being studied by Rob Naczi at Delaware State University). Although there is only one species of the pitcher-plant mosquito, it shows a great deal of variation in its life-history. In northern climates, the mosquito goes through only one generation per year, but in southern climates, it can go through two or more generations per year (Bradshaw & Louinbos 1972). As climate changes, the northern populations are responding by changing their development time, and these life history changes recently have been proposed as reliable indicators of global warming (Bradshaw & Holzpfel 2001).
In my lab, our studies to date have focused on two aspects of the pitcher-plant food web. First, we have looked at the distribution and diversity of the dominant prey, ants, in bogs throughout Massachusetts. Second, we have looked at the role that the rotifers play in providing nutrients for the pitcher plant.
What's for lunch?In contrast to the ants of grasslands, deserts, and rainforests, the ants of bogs have received little scientific scrutiny. I first became interested in bog ants when I started studying pitcher plants in 1998. Tuyeni Mwampamba, then a junior at Mount Holyoke College, conducted an in-depth study of the types of insects captured by pitcher plants at Hawley Bog, a Nature Conservancy preserve in Hawley, Massachusetts (see photo at right). Nearly 60% of the prey captured were ants, and the ant fauna was dominated by a single species, the bog specialist Myrmica lobifrons Pergande, which had not been reported previously from Massachusetts. In 1999 and 2000, Rebecca Emerson, Elizabeth Farnsworth, Nick Gotelli, Kirsten McKnight, Tim Simmons, Samantha Williams, and I conducted a state-wide inventory of the ants of pitcher-plant bogs, and found that M. lobifrons is the dominant ant species. The table below lists the ants that we found in pitcher-plant bogs (for more details on ants of New England pitcher-plant bogs, see Gotelli & Ellison 2002a and Ellison et al. in review).
| Crematogaster lineolata (Say) | Lasius alienus (Foerster) | Myrmica punctiventris (Roger) |
| Camponotus herculeanus (Linnaeus) | Lasius speculiventris (Emery) | Myrmica sculptilis (Francouer) |
| Camponotus nearcticus (Emery) | Lasius umbratus (Nylander) | Myrmica smithana (Francoeur) |
| Camponotus noveboracensis (Fitch) | Aphenogaster rudis (Emery) (s.l.) | Stenemma brevicorne (Mayr) |
| Camponotus pennsylvanicus (DeGeer) | Leptothorax ambiguus (Emery) | Dolichoderus plagiatus (Mayr) |
| Formica argentea (Wheeler) | Leptothorax curvispinosus (Mayr) | Dolichoderus pustulatus (Mayr) |
| Formica fusca (Linnaeus) | Leptothorax longispinosus (Roger) | Tapinoma sessile (Say) |
| Formica neorufibarbis (Emery) | Myrmica incompleta (Provancher) | Ponera pennsylvanica (Buckley) |
| Formica subsericea (Say) | Myrmica lobifrons (Pergande) |
|
Two of the ants, Camponotus nearcticus and Formica neorufibarbis, are boreal species and Massachusetts is near the southern boundary of their geographic range. In contrast, the more southern species Leptothorax curvispinosis reaches the northern limit of its range in Massachusetts. These three species should be closely monitored over the next decades, as changes in their geographic ranges may be good indicators of local changes in climate.
Despite their abundance in the bogs, and their dominance of the pitcher plant's diet, ants (and other prey items) account for only about 10% of the nutrients that the plant needs (Chapin & Pastor 1995, Ellison & Gotelli 2001). One of our on-going research objectives is to determine from where the plant receives the balance of its nutrients, and how pitcher plants respond to variable nutrient supply. As we move up the food web, rotifers stand out as a major contributor to the pitcher plant's nutrient budget.
Rotifers are common aquatic invertebrates, but because they are small and difficult to identify, they have received much less attention from zoologists and limnologists than other, more common zooplankton. The situation is much simpler in the pitcher-plant microecosystem, however, as there is only one common rotifer, Habrotrocha rosa, and it occurs in relatively high abundance - up to nearly 3,000 rotifers per ml (the average pitcher plant leaf holds 20 ml of water, so it could have up to 60,000 rotifers in a single leaf!) (Bledzki & Ellison 1998). Unlike many other zooplankton species, rotifers directly excrete nitrate and phosphate as part of their normal metabolic activity, and in these forms, these nutrients are directly available to the pitcher plant. Our research has demonstrated that rotifers supply four to five times as many nutrients to the plants as they derive from prey (Bledzki & Ellison 1998), so between the prey and the rotifers, we can account for about half of the nutrient budget of the northern pitcher plant. Chemical analysis of leaf tissue suggested that growth of pitcher plants was nitrogen limited (ratio of nitrogen to phosphorus in leaf tissue < 15), as would be expected in bogs where all the nutrients for plants enter the system through rainfall (or captured prey) (see Bedford et al. 1999 for a review of nutrient limitation in wetlands, including bogs). Plant growth in general is limited by some nutrient or nutrients, so it is not surprising that growth of pitcher plants also is nutrient-limited. Changing supplies of nutrients into bogs, therefore, could have a significant effect on growth of plants there.
Pitcher plants in an industrial worldPrior to the Industrial Revolution in the mid-19th century, insect prey and rotifer excreta, along with the minimal nutrients present in bog peats and pore water would have been all that pitcher plants could have counted on to meet their nutritional needs. Carnivory in plants is hypothesized to have evolved in such nutrient-poor habitats because the extra "costs" incurred by the plants in the construction of carnivorous structures would have been offset by the added marginal "benefits" gained from the extra nutrients from captured insects (Givnish et al. 1984, Ellison & Gotelli 2001). The combination of industrialization beginning in the mid-19th century and high-input agriculture of the 20th century onwards have increased the amount of nutrients, especially nitrates (NO3) and ammonium (NH4) that are emitted into the atmosphere as a result of human activities, and returned to ecosystems through rain, snow, and fog. Although implementation of the U.S. Clean Air Act has resulted in a dramatic reduction in the last thirty years of one component of acid rain, SO4, the other primary ingredient, NO3, shows little change. In fact, with more and more sport utility vehicles on the road and increasing amounts of nitrogen fertilizers being used in agriculture, the modest decline in nitrogen deposition rates observed in the late 1980s and early 1990s appears to have slowed, and deposition rates now have leveled off or are beginning to increase again (see on-line data of the National Atmospheric Deposition Program).
Northern pitcher plants essentially are small collectors of rainwater, and they accumulate whatever pollutants are transported their way by precipitation. We have taken advantage of this morphological feature to experimentally examine the effects of increased nitrogen deposition on the plants, and to determine if we can use pitcher plants as indicators of the effects of nutrient deposition on bogs. For three years (1998-2001), we experimentally altered the concentration of nitrogen (ammonium and nitrate) and phosphorus (phosphate) in a set of 90 pitcher plants at Hawley Bog. We observed and measured changes in plant size and shape, and used this information to predict how the pitcher plant populations at the bog could change under different future scenarios of changing deposition rates.
The results of our experiments were quite dramatic. Plants fertilized with nitrogen or nitrogen + phosphorus, but not those fertilized with phosphorus alone, stopped producing normal pitchers and began to produce flattened leaves, also known as "phyllodia" (see photo at right). This result supported the cost-benefit model described above for the evolution of botanical carnivory (Givnish et al. 1984). When plants were provided with surplus nutrients, as in our experiments, the benefits of being carnivorous no longer outweighed the costs of construction of pitchers, and the plants produced non-carnivorous, but photosynthetically more efficient, phyllodia (Ellison & Gotelli 2002).
The actual morphology of the leaves depended directly on the amount of nutrients supplied. In our experiments, we observed plants ranging from normal pitchers (no nutrients supplied) to complete phyllodia (high concentrations of nitrogen). Intermediate leaves — with oversized "keels" and narrow tubes — were produced when lower concentrations of nitrogen were given to the plants. We hypothesized, therefore, that we could determine how much nitrogen was arriving at a bog simply by looking at the relative size of the keel. We predicted that high nitrogen conditions would be indicated by relatively large keels, and lower nitrogen conditions would be indicated by relatively smaller keels.
We tested this hypothesis by measuring both pitcher size and nitrogen availability in bogs throughout Massachusetts and Vermont during the summer of 2000. The graph shows the results of these measurements. Between 0.1 and 1.0 mg/L of available nitrogen (as indicated by concentrations of ammonium [NH4] in the bog pore water) are reliably predicted by the relative keel size of the pitcher-plants' leaves. In Massachusetts, concentrations of nitrogen in rainfall range from <0.1 to about 0.6 mg/L, so we think we have captured the full range of nitrogen deposition with our data. On this graph, each point represents the average relative keel size of 25 leaves measured with calipers (to the nearest 1mm) on 25 different plants at each bog in July 2000. The solid line represents the best-fit linear regression, and the dotted lines illustrate 95% confidence intervals on the regression. The shape of the pitcher explains 45% of the variation in available nitrogen. This result, along with others discussed in more detail in a recent paper (Ellison & Gotelli 2002), suggest strongly that we can use pitcher plants (and perhaps other carnivorous plants) to monitor acid rain just as miners of old used canaries to monitor oxygen levels in coal mines. We observed a similar relationship between species richness of ants and nitrogen availability in these bogs. Ant species richness increased significantly with available nitrogen, illustrating that nitrogen can affect the entire bog community (Ellison et al. in review).
Based on our three years of adding nitrogen to pitcher plants at Hawley Bog, we were able to model the consequences of nitrogen deposition for pitcher plant population dynamics. The results are not encouraging. Using nutrient deposition data collected at the Quabbin Reservoir monitoring station by the National Atmospheric Deposition Program, our models predict that if there is no change in nitrogen deposition levels (relative to 1998 conditions), that the pitcher-plant population at Hawley Bog has an approximately 4% probability of extinction within 100 years, and a 95% probability of extinction in 650 years. A small (5%) increase in nitrogen deposition rates dramatically decreases, to 70 years, the time to extinction (with 95% probability), while a parallel 5% decrease in nitrogen deposition rates leads to the prediction of essentially indefinite persistence of this population (Gotelli & Ellison 2002b).
Why is it that increases in nitrogen can lead to the production of leaves with increased rates of photosynthesis but result in near-term extinction of the pitcher-plant population? The answer is based on the reproductive life history of the plant. Flower buds of S. purpurea are initiated in late summer, but development is completed the following spring when the plant finally flowers (Shreve 1906). The "decision" to flower appears to be based on how much nutrients the plants have amassed during the growing season, so plants to which we added nutrients had a greater probability of flowering the following year. However, flowering is energetically costly, and plants that flower produce 1-2 fewer pitchers than plants that don't. Under "normal" (pre-industrial) conditions, a plant that flowered in one year would have been unlikely to flower again for 2-3 more years, while it accumulated new energy reserves for another round of reproduction. Because it appears that all surplus nutrients are shunted to flowering and fruiting, continuously fertilized plants flower several years in a row. Imagine starting in year 1 with an average, adult pitcher plant with 6 pitchers. With nitrogen fertilization, in year 2, this plant will flower, but will only make 4-5 pitchers. With continued fertilization, in year 3, this plant may flower again, but will only make 2-3 pitchers. After several years, the fertilization will have burned out the plant — not the common fertilizer burn associated with too much nitrogen, but burn-out from exhaustion attendant to using up all the plant's stored resources. Although the plant may produce many seeds, the seedlings will be much more susceptible to fertilizer burning from atmospheric deposition; indeed, our observations at Hawley Bog suggest that seedlings are much less common than they ought to be, based on the size distribution and reproductive frequency of S. purpurea there.
What began as a curiousity-driven research project to study the interactions between a carnivorous plant and the invertebrate food web responsible for digesting its prey has, in a short period of time, evolved into a much broader research effort that raises significant conservation and management issues. Rather than being simple botanical oddities, pitcher plants are now seen as useful indicators of local, regional, and continental environmental change. All carnivorous plants evolved in habitats that were very nutrient-limited, but anthropogenic activities are resulting in a rapid increase in available nutrients in bogs (and, of course, upland ecosystems). Although in the short-term, pitcher plants (and perhaps other carnivorous plants) may respond to these increases in nutrients with a burst of growth, the long-term projections suggest that this burst will be followed by population collapse. Carnivorous plants merit serious attention from conservation biologists and protection from the by-products of our industrial civilization.
The research described in this review has been supported generously by grants from the US National Science Foundation (DEB 98-05722 and 98-08504), the Massachusetts Natural Heritage and Endangered Species Program (MAHERSW99-17), Mount Holyoke College, the Packard Foundation, and the Howard Hughes Medical Institute. Heidi Albright, Leszek Bledzki, Erin Cabana, Rebecca Emerson, Elizabeth Farnsworth, Nick Gotelli, Sybil Gotsch, Yvette Luvten, Krista Matthews, Kirsten McKnight, Laurel Moulton, Tuyeni Mwampamba, Jerelyn Parker, Una Pinninti, Steve Schachterle, Justine Sears, Tim Simmons, Hedda Steinhoff, Matt Toomey, Samantha Williams, and Man-yu Yum all have contributed to the ideas and participated in the field work contributing to the results presented here. Stefan Cover and André Francoeur confirmed our identifications of ants. Our research in these fragile bogs has been permitted by Five Colleges, Inc., Massachusetts NHESP, Masschusetts DFW, The Nature Conservancy, the University of Vermont, and numerous private landowners.
(In order of appearance in the article):
Pitcher plant: A. Ellison
Food web: A. Ellison (Fletcherimyia fletcheri, Wyeomyia smithii, Metriocnemus knabi), T. Miller (Habrotrocha rosa,
Sarraceniopus gibsoni, bacteria on plate). T. Linksvayer (Tapinoma sessile), N. Gotelli (Sarracenia purpurea). Montage design by A. Ellison.
Hawley Bog: A. Ellison
Pitcher plant: A. Ellison
Phyllodia: N. Gotelli
Bedford, B. L., M. R. Walbridge, and A. Aldous. 1999. Patterns of nutrient availability and plant diversity of temperate North American wetlands. Ecology 80:2151-2169.
Bledzki, L. A., and A. M. Ellison. 1998. Population growth and production of Habrotrocha rosa Donner (Rotifera: Bdelloidea) and its contribution to the nutrient supply of its host, the northern pitcher plant, Sarracenia purpurea L. (Sarraceniaceae). Hydrobiologia 385:193-200.
Bradshaw, W. E., and C. M. Holzapfel. 2001. Genetic shift in photoperiodic response correlated with global warming. Proceedings of the National Academy of Sciences, USA 98:14509-14511.
Bradshaw, W. E., and L. P. Lounibos. 1972. Photoperiodic control of development in the pitcher-plant mosquito, Wyeomyia smithii. Canadian Journal of Zoology 50:713-719.
Bubier, J. L., and T. R. Moore. 1994. An ecological perspective on methane emissions from northern wetlands. Trends in Ecology & Evolution 9:460-464.
Bubier, J. L., P. M. Crill, T. R. Moore, K Savage, and R. K. Varner. 1998. Seasonal patterns and controls on net ecosystem CO2 exchange in a boreal peatland complex. Global Biogeochemical Cycles 12:703-714.
Burr, C. A. 1979. The pollination ecology of Sarracenia purpurea in Cranberry Bog, Weybridge, Vermont (Addison County). Masters Thesis, Middlebury College, Middlebury, Vermont.
Chapin, C. T., and J. Pastor. 1995. Nutrient limitation in the northern pitcher plant Sarracenia purpurea. Canadian Journal of Botany 73:728-734.
Darwin, C. 1875 Insectivorous Plants. Appleton and Company, London.
Dörrstock, S., S. Porembski, and W. Barthlott. 1996 Ephemeral flush vegetation on inselbergs in the Ivory Coast (West Africa). Candollea 51:407-419.
Ellison, A. M. 2001. Interspecific and intraspecific variation in seed size and germination requirements of Sarracenia (Sarraceniaceae). American Journal of Botany 88:429-437.
Ellison, A. M., and N. J. Gotelli. 2001. Evolutionary ecology of carnivorous plants. Trends in Ecology & Evolution 16:623-629.
Ellison, A. M., and N. J. Gotelli. 2002. Nitrogen availability alters the expression of carnivory in the northern pitcher plant Sarracenia purpurea. Proceedings of the National Academy of Sciences, USA (in press).
Ellison, A. M., and J. N. Parker. 2002. Seed dispersal and seedling establishment of Sarracenia purpurea (Sarraceniaceae). American Journal of Botany 89: (in press).
Ellison, A. M., E. J. Farnsworth, and N. J. Gotelli. in review. Ant diversity in pitcher-plant bogs of Massachusetts. Submitted to Northeastern Naturalist.
Ellison, A. M., N. J. Gotelli, J. S. Brewer, D. L. Cochran-Stafira, J. Kneitel, T. E. Miller, A. C. Worley, and R. Zamora. 2002. Carnivorous plants as model ecological systems. Advances in Ecological Research (in press).
Fish, D., and D. W. Hall. 1978. Succession and stratification of aquatic insects inhabiting the leaves of the insectivorous pitcher plant Saracenia purpurea. American Midland Naturalist 99:172-183.
Givnish, T. J., E. L. Burkhardt, R. E. Happel, and J. D. Weintraub. 1984. Carnivory in the bromeliad Brocchinia reducta, with a cost/ benefit model for the general restriction of carnivorous plants to sunny, moist nutrient-poor habitats. The American Naturalist 124:479-497.
Gleason H. A., and A. Cronquist. 1991. Manual of vascular plants of northeastern United States and adjacent Canada. New York Botanical Garden, Bronx, NY.
Gorham, E. 1991. Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecological Applications 1:182-195.
Gotelli, N. J., and A. M. Ellison. 2002a. Biogeography at a regional scale: determinants of ant species density in bogs and forests of New England. Ecology (in press).
Gotelli, N. J., and A. M. Ellison. 2002b. Nitrogen deposition and extinction risk in the northen pitcher plant Sarracenia purpurea. Ecology (in press).
Heslop-Harrison, Y. 1978. Carnivorous plants. Scientific American 238(2):104-115.
Intergovernmental Panel on Climate Change (IPCC). 2001. Climate Change 2001: Synthesis Report. Cambridge University Press, Cambridge.
Newell, S. J., and A. J. Nastase. 1998. Efficiency of insect capture by Sarracenia purpurea (Sarraceniaceae), the northern pitcher plant. American Journal of Botany 85:88-91.
Seine, R., S. Porembski, S, and W. Barthlott. 1996 A neglected habitat of carnivorous plants, Inselbergs. Feddes Repert.106:555-562.
Shreve, F. 1906. The development and anatomy of Sarracenia purpurea. Botanical Gazette (Old Series) 42:107-126.