The Journal of Biospheric Science
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

The Official Journal of the International Biosphere Group
 

April 1999
 

Volume 1 Number 1
 
 

Editors: Mark A. S. McMenamin and Sergei A. Ostroumov
 

Welcome to the new Journal of Biospheric Science. This journal will publish articles relating to all aspects of biospheric science, particularly those continuing the research legacy of Vladimir Vernadsky. This issue's feature article is by Mark McMenamin and Jessica Whiteside, and involves the calculation of a new Vernadskian metric. This premier article is very much in accord with the stated theme of the new journal. We welcome submissions from other researchers working in the biospheric sciences. Our cover illustration shows specimens of the 550 million-year-old fossil Pteridinium from Namibia, a member of the now extinct Ediacaran Marine Biosphere or Garden of Ediacara. --Mark McMenamin
 
 

Hypermarine Upwelling and a New Vernadskian Metric
 
 

Mark A. S. McMenamin and Jessica H. Whiteside

Department of Geography and Geology

Mount Holyoke College

South Hadley, Massachusetts 01075 USA
 
 

Vladimir Vernadsky wrote (1) in 1929 that "the mass of the living organisms of the biosphere is approaching a limit . . . and the process of the occupation of the terrestrial crust by living matter is not yet completed." Our calculations indicate what one of these "limits to growth" might be for a given amount of vegetal land cover.
Adding the curves for shoot biomass and root biomass given in the caption to Figure 2 of van der Heijden et al. (2 ) yields:

y = -.069x^2 + 14.901x = 168.895

Taking the first derivative

y' = -.138x + 14.901

and solving for zero slope gives

y'(108) = 0

y(108) = 973.387 gm^-2

which we will use to estimate the theoretical maximum biomass
of the fungal-vascular part of Hypersea (3), absent accumulated woody
plant tissue.
Earth's surface area (Æ) is 2.82 x 10^7m^2; assuming that 0.167 (one sixth) of Earth's surface is potentially colonizable by vascular plants gives an aerial extent of potential vascular plant habitat of 4.7 x 10^6m^2.
Maximum hyphal length for soil fungi can be estimated
using another van der Heijden et al. (2) curve:

y = .001x^3 - .046x^2 + .756x + 2.979

y' = .003x^2 - .092x + .756

This derivative has no zero within the bounds of the data, so looking at the bounds to find extremes gives

y' > 0; x = 14

y(14) = 7.29 m/g soil

Volk (4) estimates the total surface area of fungal hyphae to be equal to six Earth surface areas (Æ). Assume that two thirds of this value represents the global surface area of mycorrhizal fungi. Then:

surface area of hyphae = 4(Æ) = 1.13 x 108 m^2

Volk (4) gives the surface area of leaves as equal to Æ. Thus, the surface area of Hypersea under optimal conditions may be conservatively estimated as the following:

Hypersea area = leaf area + mycorrhizal fungi surface area + other nonmarine fungi surface area = 2.82 x 107m^2 + 1.13 x 108 m^2 + 5.64 x 10^7m^2 =1.97 x 108m^2.

The maximum increase of translocation of phosphorus from soil to Hypersea using the curves for soil P and plant P is calculated below. The minimum value allowable for soil P can be estimated as above, namely,

y = .065x^2 - 1.593x + 14.252

y' = .130x - 1.593

y'(12.25) = 0 (minimum value)

y(0) = 14.252 mg/kg-soil

Plant P is maximized as follows:

y = 61.537x + 1156.281

y(14) = 2017.799 mg/m^2

multiplying this value by total leaf surface area gives

(Æ)(2017.799 mg/m^2) = 5.690 x 10^4 kg plant P

Assuming a soil density of 1250 kg/m^3 and a soil depth of three meters gives

Pmax = (1250 kg/m^3)(14.252 mg/kg-soil)(4P[6731000^3-6730997^3])(.1667) = 4.8 x 10^18 kg soil P

Thus the maximum increase of translocation of phosphorus
from soil to hypersea using the curves for soil P and plant
P is thus 4.8 x 10^18 kg.

This number represents the maximum vertical nutrient transport index for Earth, and represents the maximum value of hypermarine upwelling of phosphorus resulting from going from one mycorrhizal fungal species to the calculated optimum number of fungal species distributed over land. We call this value H, a new Vernadskian (1) metric for hypermarine upwelling that represents the maximum vertical nutrient transport index for our planet. There is therefore a huge amount of biomatter that could potentially be generated by ensuring that soils have a fungal diversity that optimizes hypermarine upwelling of phosphorus. This amount would approach a limit denoted by H, assuming a constant amount of vegetated land surface and adequate supplies of atmospheric carbon dioxide. Whether or not Earth's terrestrial surface will become more fully vegetated, as per Vernadsky's comment above, will involve feedback calculations linked to the hydrologic cycle.

1. Vernadsky, V. I. The Biosphere 1-192 (Copernicus, New York, 1998).

2. van der Heijden, M. G. A. et al. Mycorrhizal fungal diversity determines plant biodoversity, ecosystem variability and productivity. Nature396, 69-72 (1998)

3. McMenamin, M. A. S. and McMenamin, D. L. S. Hypersea 1-343 (Columbia, New York, 1994).

4. Volk, T. Gaia's Body 1-269 (Copernicus, New York, 1998).
 
 
 
 
 

The Birth of the Biosphere: On the Translations of Vernadsky's Work

Mercè Piqueras
 
 

The Biosphere, complete annotated edition.
By Vladimir I. Vernadsky.
Copernicus (Nevraumont)/Springer-Verlag, New York, 1998, $30.00
ISBN 0-387-98268-X

La Biosfera.
By Vladimir I. Vernadsky.
Fundacion Argentaria-Visor, Madrid, 1997, 2,700 Pesetas
ISBN 84-7774-979-5

Vladimir Ivanovich Vernadsky (1863-1945) understood the biosphere as the external envelope of the Earth, which is inhabited by living things. This comprises both all the living organisms of the planet and the elements of inorganic matter that make up their habitat. Thus, oxygen, carbon, hydrogen, nitrogen and other elements and chemical compounds involved in the vital life processes are constituent parts of the biosphere. The study of the biosphere cannot therefore be made only by biologists. To study its components and their interactions, a multidisciplinary approach is needed. However, in Vernadsky's time, nobody had even thought of interdisciplinarity. His theory was far ahead of its time. By portraying life as a global phenomenon, in which the sun's energy is transformed on Earth into a kind of "green fire," a description of photosynthesis, Vernadsky anticipated both global ecology and the concept of the "ecosystem."

For many years the only pieces of Vernadsky's writing available in English were two articles published in 1944 and 1945 in the Transactions of the Connecticut Academy of Arts and Sciences and American Scientist, respectively. The first English edition of The Biosphere, published by Synergetic Press (Arizona) came out in 1986. Like the French source from which it had been translated, this edition was an abridged version. Nevertheless, it served a valuable function, since it allowed English-speaking audiences direct access to Vernadsky's most famous piece of writing. Well before publication of the Synergetic Press edition, a typescript of an entire English version of The Biosphere circulated among Vernadsky's American followers. Science editor Peter N. Nevraumont rescued that translation which, in 1998, was finally published by Copernicus Books of Springer-Verlag. Almost at the same time, the Spanish La Biosfera was published by Fundacion Argentaria, in its series "Economia y Naturaleza" (Economy and Nature).

These two new translations of The Biosphere both have particular features that make them milestones in scientific publication. The American edition is the first published English translation of the entire text and includes author's prefaces to both the 1926 Russian edition and the 1928 French edition. American geologist Mark A. S. McMenamin gives extensive, accurate annotations to explain the structure of Vernadsky's arguments. The book also includes a foreword co-signed by an international panel of scientists that share an interest in global biological issues. An excellent introduction, "The invisibility of the Vernadskian revolution", by Swiss philosopher and science historian Jacques Grinevald, places the book in its historical context. The book has two appendices; a biographical chronology of Vernadsky, compiled by Grinevald and a list of Vernadsky's publications in English, compiled by A. V. Lapo. An extensive bibliography is also included. Grinevald, who has been instrumental in disseminating Vernadsky's thought and works, has also contributed a very useful chronology of the Russian researcher to the Spanish La Biosfera. The seventeen pages, besides making the reader acquainted with the Russian scientist's life, describe the development of Vernadsky's scientific thought. Additional work by Vernadsky is also contained in the book: the text of a lecture given to the Society of Naturalists of Leningrad in 1928, and the American Scientist article entitled "The biosphere and the noosphere" published in 1945. The Spanish edition is unusual in that institutions dealing with financial activities rarely publish scientific books, particularly ones written by foreign authors who have been dead for over fifty years and dealing with a subject apparently far from economics. However, the more one knows about ecology and economics, the more similarities one can find between these two disciplines.

Among the best pages in the Spanish La Biosfera is the ten-page introduction by Professor Ramon Margalef of the University of Barcelona. He comments on the obsolete aspects of Vernadsky's work, but also praises the freshness and current interest of some of his ideas. He acknowledges the value of the book, which offered for the first time a planetary vision of life. As with most of Margalef's writings and lectures, his text sparkles with wit and erudition, not to mention piercing criticism of the current lack of interest for popular science in Spain. Margalef recalls with affection the 1930s trend for good Spanish translations of seminal books by creative authors, mainly on physics and biology. He finally expresses his wish that La Biosfera make its readers reflect on the history of ideas, on the conflicts that come and go with time, and on the reciprocal influences that should be promoted between disciplines.

[Versions of this review appeared in International Microbiology (1998) 1:165-170 and Gaia Circular (1998) 1(2):13]
 
 

Evolution of Consciousness in the Context of Biosphere

Alexei Ghilarov

Metaecology: Regularities in the Evolution of
Natural and Mental Systems [in Russian]
By Valentin Krasilov
Paleontologicheskii Institut RAN, 1997, 208 p.

The general anxiety about clonal sheep Dolly clearly indicates that we are well aware both of our likeness to other animals and of the fact that we are descended from ape-like ancestors. However we still believe that one character sharply delimits humans from other living beings. This is of course our well-developed consciousness, that cunning apparatus allowing us to use external sources of energy and matter with great efficiency. Although almost nothing is known about the origin of consciousness of our ancestors, it would be generally admitted that this ability underwent some type of evolution. To reconstruct the course of biological evolution, scientists use paleontological evidence as well as vast material supplied by morphology, embryology and molecular biology. If there is such a thing as the evolution of consciousness one can suppose that some vestige of this process must still exist. Perhaps these vestiges are all around us, but being highly dispersed and embedded in familiar contexts they are not readily discernible.

The author of Metaecology, well-known paleobotanist Valentin Krasilov attempts to reconstruct the general pattern of the evolution of consciousness, drawing special attention to the relations between developing personality and its mental environment - the world of notions and ideas that always surround any human being. One of the essential statements of Krasilov's concept is the simple proposition that human consciousness is at the same time a product and a part of natural evolution, and therefore, its analysis in the framework of an evolving biosphere holds promise. Another of Krasilov's founding principles is the statement that all open (in thermodynamic sense) systems are similar in their development aimed at the decrease in entropy production. As natural ecosystems evolve there is an increase in efficiency of creating living matter from inert material of environment, that can be exemplified by the changing ratio of living biomass to mass of dead organic matter. The essential condition of such long-term changes is the increase in biological diversity due to the specialization of organisms and reduction of niche overlap. The process of biological evolution from time to time results in "inventions" (e.g. photosynthesis, capacity to maintain constant body temperature, mind) that allow organisms to stabilize their environment and, therefore, benefit from the results of such stabilization to reduce competition and decrease the redundancy of their populations (i.e. producing the "excess" of newborns in the face of great mortality). For early humans the impact of natural selection as the survival of the fittest in harsh environments gradually diminished while sexual selection (choosing of the mate) and cooperation became more important. As Krasilov remarks, the use of fire and improved dwellings was aimed more at the support of weak and vulnerable individuals than at the maintenance of the strongest. The development of primitive society and culture leads to the creation of new niches and to the weakening of competition. Using their great abilities to stabilize the environment, people can in principal provide for the stable development of the whole biosphere. Krasilov adds that the negative effect of the present human impact on nature doesn't necessarily contradict such a view, because current environmental problems are primarily due to the relative youth of our civilization.

The emergence of self-consciousness is considered the result of systemic changes caused by the need to acquire the mechanism of internal regulation and hence to maintain the general stability of the system. Similar mechanisms of internal regulation also exist at other levels of life organization. Thus, for the genome it is molecular editing that cuts off the defective parts of DNA; for populations, sexual selection (while the natural selection serves as an external regulator); for developing personality, regulation by self-consciousness. The focusing of every intellect not only outwards, to the external word but also inwards, to its own behavior, leads to the evolution of a special structure which we call the inner world of a person. "Split personality", as the author remarks, is characteristic to some extent for every creative personality because reflection is required to develop the creativity. Therefore, here is the origin of the theme of twins, a duality so fully elaborated in mythology and so thoroughly explained in Krasilov's book.

The transformation from conflict to cooperation is considered a general trend of evolution. Thus, the author supposes that interactions between nucleic acids and proteins particles might have originated as some form of molecular parasitism but that later, nucleic acids became programming devices that were able to reproduce their protein covers. For humans we must accept a model of optimal relations with surrounding world. Krasilov believes that the appearance of mind in the course of evolution was induced by systemic goals, and since mind can store and process information about the biosphere it might be useful for its further maintenance. Biospheric ethics, although an emergent area of thought, already demands from humanity a clear understanding of its general goals. These goals themselves are products of general evolutionary trends.

It worth noting that Krasilov sometimes uses unusual terms but these are clearly defined in a special glossary, and thus the usage of these terms does not create special difficulties for the reader. For example, "metaecological system" in Krasilov's parlance is "the system of relations between personality and its mental environment"; "metaecology" means "the study of metaecological systems", while the "egosystem" is considered as the pattern of development of individual spiritual life". The titles of some chapters may appear esoteric in a book written by a professional biologist (e.g. "Presentiments", "Twins", "Crossing", "Struggle", "Egosystem"), but the writing of the Russian text is quite good and the general style of presentation is very readable. Certainly this is not traditional scientific writing but is rather an essay written with great freedom of expression. Some readers may dislike this approach, but those who are not put off by this book's unfettered style will find it instructive and a stimulus to further thought and reflection. This book deserves to be more widely known and certainly merits translation into English.

[Alexei Ghilarov is in the Department of Vertebrate Zoology and General Ecology, Biological Faculty of M. V. Lomonosov Moscow University, Moscow 119899, Russia]
 
 
 

The Cambrian Ecotone: Dynamics of a Major Evolutionary Discontinuity
 

Mark A. S. McMenamin
 
 
 
 
 

[Mark McMenamin is at the Department of Geography and Geology, Mount Holyoke College, South Hadley, Massachusetts 01075, mmcmenam@mhc.mtholyoke.edu]
 
 

October 1999
 

Volume 1 Number 2 **under construction**
 
 

Water Self-Purification and Natural Bioremediation in the Biosphere: New Concepts and New Experimental Data

S. A. Ostroumov
 

Key words: marine ecosystems, freshwater ecosystems, biosphere,  filter-feeders, filtration, clearance rate, self-purification, bioremediation, pollution, bivalves, mussels, pollutants, contaminants, surfactants

ABSTRACT

Some approaches to the definition of the phenomenon of the biosphere assume that the key attribute is the ability of the system to perform such holistic functions as self-regulation and self-support. We consider aquatic ecosystems an integral and important component of the biosphere. One of the holistic functions of aquatic ecosystems is their cleaning the water via a multitude of various mechanisms. The aim of this paper is to present some rudiments of the theory of ecosystem self-purification which emphasize the importance of several functional biological filters that are instrumental in purifying and upgrading the quality of water in aquatic ecosystems. Among the most important functional filters are: (1) direct water filtering by aquatic organisms that are filter-feeders; (2) the filter (represented mainly by communities of aquatic plants/periphyton) which prevents input of pollutants and biogenic elements (N, P) from land into water bodies; (3) the filter (represented by benthic organisms) which prevents re-entry of pollutants and biogenic elements from the bottom sediments into the water; (4) the filter (represented by microorganisms attached to particles suspended in the water) that provides microbiological treatment of the water column. New experimental  results by the author reveal the role of man-made effects on the ecological machinery which purifies water (Ostroumov, 1999a-f). This paper includes some theoretical analysis and discussions which pave the way for the holistic theory of the process of  natural bioremediation in marine and freshwater ecosystems.
 

1. INTRODUCTION

Stability of the biosphere includes several important components. One of them is self-supporting stability of aquatic ecosystems, which includes maintaining the purity of water. Ecosystems are capable of removing polluting substances from water through a variety of physical, chemical and biological processes (e.g., Gehm and Bregman, 1976; Konstantinov, 1979; Grice and Reeve, 1982; Skurlatov, 1988; Izrael and  Tsyban, 1989; Tilzer and Serruya, 1990; Beyers and Odum, 1993; Horne and Goldman, 1994; Koronelli, 1996;  Ostroumov et al., 1997; 1998; Sommer, 1998). The complex network of these processes is vital to upgrade and maintain the quality of water compatible with providing habitats for a number of aquatic species. Another group of important processes are those which remove excess biogenic elements (primarily N, P) from water or prevent them from being accumulated in water at concentrations above certain levels (e.g., Kairesalo and Seppala, 1987; Robach et al., 1991; Rogers et al., 1995; Duarte and Sand-Jensen, 1996; Stimson et al., 1996; Mandi et al., 1996). The entire system of all these processes is important to maintain a certain level of purity of water, which is an extremely significant condition for making natural water of many water bodies a resource for human consumption. The role of surface water bodies as a resource (vs. groundwater) varies in different regions but  is generally significant. Also, the role of natural self-purification is important in maintaining habitats for biodiversity of aquatic organisms, many species of which are under threat from habitats deterioration (Yablokov, Ostroumov, 1983, 1985, 1991). The latter was indicated as one of causes of the fact that 93 species of zoobenthos are endangered in some parts of the Wadden Sea, 71 species are endangered in the entire Wadden Sea, and 7 species are possibly extinct in the sea (Petersen et al., 1996). Given the total number of species of macrozoobenthos ca. 400 (Petersen et al., 1996), it means that the percentage of species which are to some extent  endangered is ca. 20-25 %, a matter of serious concern. In order to verify our understanding  the water purification in aquatic ecosystems, some useful models have been developed (e.g.,Vavilin, 1983; 1986).
    The aim of this paper is to analyze key data on various aspects of ecology of organisms which participate in water purification, towards better understanding ecosystem processes that  are instrumental in purifying and upgrading the quality of water in aquatic bodies.
This paper is based in part on the presentations given by the author in the Institute of Freshwater Ecology (Berlin) and Procter & Gamble (Brussels) in 1998.

2. DIVERSITY OF PROCESSES AND MECHANISMS CONTRIBUTING TO WATER PURIFICATION

A great many of various groups of organisms contribute to the processes leading to self-purification of aquatic ecosystems. The relevant literature is enormous and mentioning even the most recent publications is beyond the scope of this paper. Among the contributing organisms are bacteria  (e.g., Van Beelen and Van Keulen, 1990; Visscher and Taylor, 1993, Beyers and Odum, 1993, Koronelli, 1996), protozoa (e.g., Beyers and Odum, 1993), microalgae (e.g., Wilkinson et al., 1989; Sirenko, 1990; Braginskij et al., 1994; Bjork and Gilek, 1997),  macroalgae (e.g., Haglund and Lindstroem, 1995; Moy and Walday, 1997), vascular  plants (macrophytes) (e.g., Liu and Seki, 1988; Robach et al., 1991; Mandi et al., 1996), various invertebrates (see below).
    Examples of various processes leading toward upgrading the quality of water and its purification are given in Table 1.
In addition to the summary of the processes and factors leading to the self-purification of an ecosystem, it is noteworthy to consider some elements or structural blocks of aquatic ecosystems which perform part of the functions contributing to the final self-purification. On the basis of abundant literature (e.g., Gehm, and Bregman, 1976; Konstantinov, 1979; Koronelli, 1996) and our works (e.g. Ostroumov, 1986; Telitchenko and  Ostroumov, 1990; Beyers  and  Odum, 1993; Ostroumov and Donkin, 1997; Ostroumov at al., 1997; 1998; Sommer, 1998), it is useful to consider several  functional biofilters which serve as components for the entire self-purification process (Table 2).
    The most important biofilter is the sum total of filter-feeding aquatic animals. Among them are bivalves, crustaceans, rotifers, some protists, bryozoans, tunicates, and other organisms (e.g., Schroder, 1987; Konstantinov, 1979; Alimov, 1981; Ghilarov,  1987; 1990; Officer et al., 1982; Lindeboom et al., 1989;  Loo and Rosenberg, 1989; Hily, 1991; Sommer, 1998; Welker and Walz, in press)  Some aspects of this type of ecosystem biofilter are analyzed in the next section. Filter-feedeers are a very important factor to regulate a variety of parameters and processes in aquatic ecosystems. Among many aspects of their contribution to the well-being of the ecosystems, it is worthwhile to mention their ability to contribute to removing algae from the water and to preventing the ecosystem from  a rapid eutrophication. The evidence for the high efficiency of various filter-feeders in the role of the natural control factor on phytoplankton and eutrophication was obtained by several independent laboratories which worked on marine (Officer et al., 1982; Lindeboom et al., 1989;  Loo and Rosenberg, 1989; Hily, 1991) and freshwater ( Welker and Walz, in press) ecosystems. In the paper by M.Welker and N.Walz  the ecosystem of the Krumme Spree (a 21 km long reach of the river Spree, Germany) was studied. The bivalve community of the river was represented by unionid mussels (Anodonta anatina, Unio crassus, Unio pictorum) and zebra mussels (Dreissena polymorpha). The total biomass of bivalves was more than 11 metric tons of the  DW (dry weight) (shell free), i.e. at average about 20 g DW per square m. The total filtration rate was estimated at over 300,000 cubic m per day, and the total clearance rate of bivalves during the residence time  in the Krumme Spree was calculated as 14.9 - 82.3 % of the volume. The total loss in phytoplankton biomass in the Krumme Spree  varied from 269 to 4059 kg DW/day (at various days of the time interval between 6th June and 12th September).
In marine ecosystems, high efficiency of the filter-feeders in removing phytoplankton from the water column was shown, e.g., in Laholm Bay (in the Kattegat), dominated by the suspension-feeding bivalves Cardium edule and Mya arenaria ( Loo and Rosenberg, 1989), in Chesapeake Bay where importance of oyster (Crassostrea virginica) was emphasized by several authors (e.g., Ulanowicz et al., 1992), and for a variety of filter-feeders, e.g.,  in the Bay of Brest, France (Hily, 1991) and  in the western Wadden Sea (Lindeboom et al., 1989).
    The second biofilter is represented by the organisms that may prevent or slow down the flow of pollutants, organic matter and biogens from the land surrounding the water body into the water (e.g., Kairesalo and Seppala, 1987; Robach et al., 1991; Mandi et al., 1996). This type of biofilter is comprised of aquatic vegetation next to the shores and the rich community of invertebrates and microorganisms associated with these plants. Biogenes which enter the water (e.g. fertilizers or products of nitrogen fixation by soil microorganisms) may become taken up by the aquatic vegetation and serve the trophic chains based on it. As a result, a significant part of the biogenes may become accumulated and recycled within the community of peripheral aquatic vegetation, instead of entering the main part of the water. As an example, the study of various hydrosystems of the Rhine River and the upper Rhine valley have shown that the best results for self-purification were observed in the old braids and that the aquatic macrophyte communities were involved (Robach et al., 1991). Another example was assessing the efficiency of a Phragmites australis system in water purification (Mandi et al., 1996). One of the systems was represented by a bed of 50 m in length, with a horizontal water flow  of 10 L /s. Retention time varied between 1 and 4 h. The decrease in organic load (COD), nutrients  (total Kjeldhal nitrogen, TKN, and total phosphorus, TP), and parasitical load (helminth eggs) was very sharp in the bed (COD: 62%, TKN: 43 %; TP: 14%;  helminth eggs: 93%). Mean aerial productivity of the studied reed bed was estimated at ca. 134 tons DW/ha (Mandi et al., 1996). The significant role of periphyton in P removal from water was shown in studies of  mesocosms at  a Finnish lake (Kairesalo and Seppala, 1987). Over 20 % of phosphorus added to the mesocosms (volumes 70 and 410 liters) was bound by the community of periphyton in the littoral ecosystem of the lake (Kairesalo and Seppala, 1987).
    The third biofilter may decrease or partially prevent the re-entry of chemicals from the bottom sediments into the water column (e.g., Rogers et al., 1995; Duarte and Sand-Jensen, 1996; Stimson et al., 1996). The flow of phosphorus from the sediments to water in the northern high productive region  (192 km2) of the Japan Sea was estimated  as high as 1.3 metric ton per day, in another region (3234 km2) - about 15 ton per day (Endo et al., 1987). In Lake Michigan, the release of phosphorus from sediments into water is  1.4 - 56  micromole P per m2 per hour (Larsen et al., 1994). The function of this biofilter is performed by the diverse complex of benthic organisms, including benthic plants. The importance of this function is evident when it is taken into consideration that the sediments are the storage place for both pollutants (e.g. heavy metals and persistent organics) and the biogens. At the expense of light as the sourse of energy as well as some chemical reactions, the benthic organisms grow and absorb biogens leaking from the sediments and/or the bottom layer of water. As a result, the biogens are accumulated into the biomass of benthic organisms instead of being immediately released into the water. Thus, benthic organisms bind up part of the biogens and by doing so decrease the reverse flow of them into the water. Also, the benthic  macrophytic community and microorganisms supported by it may contribute to binding and destroying pollutants that are leaking out from the sediments or dissolved in the water surrounding the macrophytes.
    It was shown that the availability of nitrogen as a sediment nutrient was a crucial factor for growth of wild celery Vallisneria americana Michx. in Lake Onalaska, Wisconsin (Rogers et al., 1995). In another study, it was shown that the shoot of the seagrass Cymodocea nodosa Ucria (Aschers.) in the shallow Alfacs Bay of the Spanish Mediterranean coast play a role of a storage site of phosphorus depending on the availability of this element from the sediments (Duarte and Sand-Jensen, 1996). The ability of macroalgae to respond to availability of anthropogenic nutrient (nitrogen and phosphorus) input and to the nutrient regeneration from sediments beneath thalli was shown in the studies of the green macroalgae Dictyosphaeria cavernosa (Forskaal) Borgensen in Hawaii (Stimson et al., 1996).
    The ability of macrophytes to absorb such pollutants as heavy metals was shown in the studies of Ceratophyllum demersum L. (e.g., Parfenov, 1988). This species can accumulate Pb in proportion to its content in the water, up to 4.8 mg/g (dry biomass) at the Pb concentration in  water of  mg/L (Parfenov, 1988). Aquatic macrophytes can remove some organic pollutants  (e.g. triphenyl methane  dyes) from the water, too (Timofeeva and Cheremnyh, 1988).
    The fourth filter is associated with slowly sedimenting microorganisms which are in part aggregated or attached to particles suspended in water (e.g., Konstantinov, 1979; Izrael and Tsyban, 1989; Inkina, 1987;  Logan and Hunt, 1987; Otsuki et al., 1988). This type of filter is in part functionally analogous to pumping water through a biotechnological device called a bioreactor (e.g., Ostroumov and  Samojlenko, 1990). The latter is made up of microorganisms (e.g., Pseudomonas mendocina - see Ostroumov and  Samojlenko, 1990)  immobilized on fibers or on other surfaces; the microorganisms remove and biodegrade pollutants from the water. However, in the case of a natural ecosystem it is not water moving along microorganisms that remain stationary, but vice versa; it is microorganisms that move though the relatively stable water column. The movement of microorganisms is driven by gravitational force, and the movement is sped up by the attachment of bacteria to the bigger particles or aggregates which are suspended in the water (e.g., Izrael and Tsyban, 1989; Sadchikov, personal communication). The fact that a significant number of functionally active bacteria are attached to various sedimentary particles and pellets is well-documented (e.g., Konstantinov, 1979; Izrael and Tsyban, 1989; Sadchikov, personal communication). Some specific examples include lakes (e.g., Lake Constance - see Simon, 1988;  the Narochan lakes - see Inkina, 1988), estuaries (e.g., the Fraser River Estuary, British Columbia - see Otsuki et al, 1988), and seas (e.g., Logan, and Hunt, 1987).
It should be noted that the biological filters are only a part of the ecological machinery of water self-purification. The most important functional parts of that machinery are such chemical mills as the processes of microbiological and exoenzymatic degradation of pollutants and such functional export pumps as removals of pollutants through the volatization and sediment sorption. Additional process such as the export of the biogenic elements (N, P) are associated with the removal of some biomass from aquatic ecosystems (through predation on aquatic organisms and the natural process of the methamorphosis of the larvae and pupae of Diptera and other insects with aquatic larvae).

3. DOES POLLUTION INFLUENCE THE PROCESSES OF WATER PURIFICATION?

There are several aspects of self-purification that are vulnerable to inhibitory actions of pollutants. We will mention here only two of them, both of which are of great importance. These are: (1) effects of contaminants on microorganisms; (2) effects of contaminants on filter-feeders (e.g., Ostroumov et al, 1997; 1998).
    As far as aquatic microorganisms are concerned, there is a good body of evidence that contaminants may inhibit their ability to degrade the dissolved organic matter. It has been shown that a number of metals inhibit the bacterial degradation of amino acids in the natural water in the Rhine River. The bacterial toxicity followed the order Hg > Ni > Cu > Pb > Cd > Cr > As (Roth et al., 1992).
Also of great importance is the contaminant-induced disturbance of filter-feeders. Water filtering by filter-feeding invertebrates is an extremely important process which influences at least eight other important processes in the ecosystem, all of which are relevant to physical, chemical and biological aspects of water purification (Ostroumov et al., 1997). Among these are: (1) filtering-induced decrease in the amount of suspended particulates; (2) increase in the transparency of the water column; (3) increase in sunlight and UV penetration into the water; (4) regulation of the plankton species composition and in particular (5) removal of various microorganisms (see Table 3); (6) generation of pellets of faeces and pseudofaeces; (7) increasing aeration of water column through improved mixing; (8) acceleration of the process of sedimentation of particulate organic matter in the direction of the bottom and increased accumulation of organics in the sediments. The latter process is important not only for water purification but also for the biogeochemical flow of carbon from the atmosphere to the benthic deposits of C and, hence, for the CO2 balance in the atmosphere (e.g., Zavarzin,  1984;  Lovelock and Kump, 1994).
    Our data, as well as that found in the literature, give several examples of how pollutants may inhibit the filtering activity of aquatic organisms. The pollutants excercising such effects are as diverse as metals (Cu, Cd, Zn, Ni, Hg, Cr, Mn), pesticides, oil and surfactants (Table 4). In addition, it is known that increasing concentrations of particulates suspended in water also inhibits the filtering rate of various aquatic invertebrates (e.g., Alimov, 1981).
    The organisms susceptible to such effects are diverse and include bivalves (e.g. Ostroumov et al., 1997), rotifers and many others. Studies of the effects of synthetic surfactants on water biofiltering by the mussel Mytilus edulis demonstrate pronounced effects of  an anionic (Table 5) synthetic surfactant. We have shown (Ostroumov and  Donkin, in preparation) that the non-ionic surfactant, Triton X-100, inhibited water filtering by M. edulis. Following  the 60-min filtering period, the number of cells of algae Isochrysis galbanaobserved in beakers with 1 mg/L Triton X-100 was 3143 cells per 0.5 mL, which was over twice as many as the number of cells in  control beakers without any additions of the surfactant. In the control beakers the concentration of cells was  1330 cells per 0.5 mL (Ostroumov and Donkin, in preparation).
    In addition, our studies demonstrated the inhibitory effects of cationic surfactant tetradecyl trimethyl ammonium bromide (TDTMA) on water biofiltering by the rotifer Brachionus angularis (Kartasheva and Ostroumov, 1998). At the concentration of 0.5 mg/L, TDTMA inhibited the average filtering rate of B. angularis so that it was 44.7% - 72.3% of the control on average over the period of filtration 120-285 min, at temperatures 22°C - 24°C. Some other components of the water-purifying machinery of aquatic ecosystems are also susceptible to potential impairments from environmental pollution (see Table 6; also, some new data, e.g. [McCutcheon, Ostroumov, 1999; Ostroumov, 1999 d; 1999e; 1999 f; Ostroumov et al., 1999; Weiner, Ostroumov, 1999]). The new data are relevant to understanding how biodiversity contributes to the stability of the biosphere (Yablokov and Ostroumov, 1983; 1985; 1991). Our analysis is a step toward an integrating theory of natural bioremediation of aquatic ecosystems.

4. CONCLUDING REMARKS

 1. The complex ecological machinery which performs water purification in aquatic systems includes at least four types of functional biofilters, consisting of, respectively, aquatic bacteria, algae, plants, and invertebrates.
 2. One of these four types of functional biofilters is represented by invertebrates which are filter feeders, e. g. bivalve molluscs and other organisms.
 3. An additional aspect of ecological risk from pollutants is their ability to inhibit the water filtering rate and, by doing so, to impair a set of processes leading to water purification.
 4. New evidence in support of the above conclusions was obtained in experiments conducted by the authors. New evidence testifies to the ability of synthetic surfactants, which may enter water bodies as pollutants (Ostroumov, 1986, 1990, 1991; 1999 a-f), to inhibit water filtering by bivalves and rotifers.
 5. A better understanding of the machinery of self-purification in aquatic ecosystems is a pre-requisite for better understanding the structure and functioning of aquatic ecosystems (e.g., Ghilarov,  1987; 1990; Fedorov, 1979) and the connection between the functioning of aquatic ecosystems and global biogeochemistry (Zavarzin, 1984; Lovelock and Kump, 1994).

5.ACKNOWLEDGEMENTS.
The research was supported by the International Biospherics Group (IBG). The author is grateful to Dr. Peter Donkin (Plymouth Marine Laboratory) for hosting and helping his work with mussels; Dr. A.G. Dmitrieva for reading and discussing fragments of the first version of the manuscript, Prof. Ch. Steinberg, Prof. N. Walz, Academician M.E.Vinogradov,  Prof.V.D.Fedorov, Prof.V.N.Maximov, Dr.O.F.Filenko, and Martin Welker for discussions; Mr. Glenn Kempf for reading  fragments of first drafts of the manuscript and discussions, Dr. T.A.Ostroumova for helping in preparing some parts of the manuscript. Part of experimental research which was a basis for this paper was sponsored by EERO (European Environmental Research Organization). The final phase of the work was in part supported by MacArthur Foundation and the Open Society Support Foundation (RSS, grant  No. 1306/1999).

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 Table 1. Some examples of processes and factors instrumental in purification and  upgrading the quality of water in  ecosystems (e.g., Gehm, Bregman ,1976; Konstantinov, 1979; Grice and Reeve, 1982; Yablokov, Ostroumov, 1983; 1985; 1991; Ostroumov, 1986; Skurlatov,1988; Telitchenko, Ostroumov, 1990; Tilzer and Serruya, 1990; Beyers, and Odum, 1993; Lee et al., 1993; Koronelli, 1996; Lorenz et al., 1996).

Types of processes Some examples of processes and factors

1.Physical 1.1.Dilution;
1.2.Adsorption;
1.3.Sedimentation;
1.4.Evaporation
2.Chemical 2.1.Hydrolysis;
2.2.Photochemical reactions;
2.3.Oxydations;
2.4.Free radical-dependent destruction;
2.5.Complexing by and binding to other molecules
3.Biological 3.1.Microorganism-dependent oxidation and destruction;
3.2.Filtering  water by filter-feeding organisms;
3.3.Adsorption on biological particles;
3.4.Sorption and binding by organic matter of biological origin;
3.5.Inactivation of pathogenic microorganisms by chemical substances excreted by algae and  other organisms

 Table 2. Some types of functional biofilters and organisms involved in water self-purification

No Types of functional biofilters Examples of organisms involved References (examples)
1 Direct water filtering by aquatic organisms which are filter-feeders Bivalves, Crustaceans, Rotifers, Protists etc. Ghilarov, 1987; 1990;
Gutelmaher, 1986;
Sushchenya, 1975;
Alimov, 1981;
Joergensen, 1990
2 Biofilter which prevents input of pollutants/biogenic elements from the land into the water bodies Aquatic plants adjacent to the shores and the whole community associated with these plants Konstantinov, 1979; Mandi et al., 1996;
3 Biofilter which prevents re-entry of pollutants and biogens from the bottom sediments into the water column Benthic organisms, esp. phytobenthos Konstantinov, 1979
4 Biofilters which exercise microbiological treatment of the entire water column in situ Bacteria, fungi, algae attached to the particles which precipitate from the surface of water towards the bottom Ostroumov, 1986;
this paper
 Table 3. Removal of microorganisms from water by filter-feeders (examples)
Filter-feeder species Microorganisms which were shown to be removed from the water References
Bivalves Mytilus galloprovincialis yeast Saccharomyces cerevisiae New data by the author
Bivalves Venus verrucosa Escherichia coli Charles, 1994
Bivalves Crassostrea gigas, Perna viridis, Marcia japonica, Scapharca cornea, Geloina erosa E.coli Kueh, 1987
The Baikal sponge Lubomirskia baicalensis Yeasts and spores of bacilli Gil et al., 1997
 

Table 4. Inhibitory effects of water contaminants and pollution on the rate of filtering by aquatic organisms (examples)
Types of pollutants Organisms References
pesticides Mytilus edulis Donkin et al., 1997;
surfactants Mytilus gallprovincialis New data by the author
surfactants Mytilus edulis Ostroumov et al., 1997;
Cu, Cd, Zn Dreissena polymorpha Kraak et al., 1993
Ni Dreissena polymorpha Stuijfzand et al., 1995;
Cationic surfactant TDTMA rotifer Brachionus angularis Kartashova and Ostroumov, in preparation
Particulate matter (water suspersions) various filter-feeders various authors
Cd, Zn, Cu Crassostrea gigas Lin et al., 1992; 1993;
Hg, DDT Mitilus galloprovincialis Krasota and Kostylev, 1988;
Cr, Mn, Ni, Cu,Cd, Hg bivalve Villorita cyprinoides Abraham et al., 1986;
Kuwait crude oil bivalve Venus verrucosa Axiak, George, 1987;
Cd pocketbook mussels (freshwater) Lampsilis ventricosa Naimo et al., 1992;
 Table 5
Anionic surfactant SDS inhibits water filtering by mussels Mytilus edulis. The effect is measured as decrease in  Isochrysis galbiana cell density  (per 0.5 ml) during filtering by Mytilus edulis at 1 mg/L SDS (After Ostroumov et al., 1997, with some changes).

 Experimental beakers Control beakers
Time
after ad-
ding algae,
min Cells
count
in indivi-dual beakers
(experi-mental,
+SDS) Cells
count,
average
(experi-mental)
A StandardError Cells count
in indivi-dual
beakers
(control, no SDS)

 Cells
count,
average
(control)
B Standard
Error Ratio
A/B
5 18521
16959.7
17087.7
17194.7 17440.8 363.27 21230.7
14679.3
16946.7
16807.3 17416 1373.3 1.001
35 9559.7
6775.3
5080.3
4958 6593.33 1072.22 7242
3146.7
4676.3
4461.3 4881.58 856.36 1.351
65 4440.3
2169.7
1117.7
1068.3 2199 789.1 1767.7
581.7
1021
989 1089.83 247.08 2.018
95 2226
1122.3
308.7
355 1003 448.33 521.3
196
371
392.7 370.25 66.89 2.709
Cell density at the beginning of the experiment: 19533 per 0.5 ml.
Average Coulter count in filtered sea water:  131.7.

Table 6. Components of water-purifying system that are susceptible to environmental pollution (some examples)
No Organisms as components of a water-puridication system Type of biofilters they may belong to, according to Table 2 Examples of recent studies - effects of pollutants on those organisms
1.  Bacteria 2,3,4 Ostroumov and Weiner (in press)
2.  Cyanobacteria 2,3,4, Waterbury and Ostroumov, 1994;
3.  Green algae 2,3,4 Goryunova and Ostroumov, 1986;
Maximov et al., 1988;
Ostroumov, 1994a; 1994b;
4.  Diatoms 3,4 Ostroumov and Maertz-Wente, 1991; Fisher et al., 1996;
5.  Vascular plants 2 Ostroumov, 1990; 1991; 1994a; 1994 b;
Ostroumov et al., 1994;
6.  Invertebrates 1 Lin et al., 1993;  Stuijfzand et al., 1995; Donkin et al., 1997; Donkin and  Ostroumov, 1997;
Ostroumov and Donkin, 1997;
Ostroumov et al., 1997; Endo T.

[S.A.Ostroumov is in the Department of Hydrobiology, Faculty of Biology,  Moscow University, Moscow 119899, Russia;
email: saostro@glas.apc.org]
 
 

May 2000
 

Volume 2 Number 1
 
 

Pollination and Fruiting Success in the Eastern Skunk Cabbage
 Symplocarpus foetidus (L.)  Salisb. ex Nutt.
 

Katherine K. Thorington


ABSTRACT

            In an eighteen-month study of the pollination and fruiting success of the eastern skunk cabbage, Symplocarpus foetidus, the life history and pollen transport mechanisms were investigated. Potential pollination mechanisms include invertebrate activity and wind. In February of 1999, I marked 137 reproductively active plants in two sites on the Mount Holyoke College campus. These sites included sections of streams that run year-round as well as seeps that become progressively drier throughout the growing season. Reproductively active plants were defined as those with at least one inflorescence. These inflorescences bloomed between February and April of 1999. Plants had one to four inflorescences with a per plant average of 1.7 inflorescences. These marked plants were followed through August 1999 and a subset, including those plants that bore fruit in the summer of 1999, were followed through April of 2000. Other plants treated with tanglefoot insect glue to trap pollen and invertebrates were investigated to determine to what extent pollen is airborne versus invertebrate-borne. Invertebrates found in these inflorescences were isopods, arachnids and insects. The insects included orders Plecoptera, Diptera, Protura, Collembola and Thysanoptera. Of the 226 inflorescences followed in 1999 only 14 successfully became mature fruit. Sites were statistically different in numbers of inflorescences per plant (C2 =12.2 p= 0.005), numbers of fruit (C2 = 4.6 p= 0.05), and numbers of invertebrates in glue treated inflorescences (p = 0.01, ANOVA). Insects are most likely the most effective pollination vectors of S. foetidus.

INTRODUCTION

Pollination  
    
    Reproductive success in plants may be limited by many factors, including water, nutrients, light, space, pollen and pollinators. In terrestrial flowering plants, once the process of reproduction begins, one of the first problems an individual encounters is how to develop male and female gametes in the same fertile state at the same time and place. Pollen-limited plants have low fertilization due to a lack of pollen. A lack of pollen could result if pollen availability differs from floral receptivity, or it could be due to low pollen count where there is not enough pollen produced to pollinate the flowers. Pollinator-limited plants have lots of pollen but little or no system to transport their pollen (Kearns and Inouye 1993). Angiosperms have developed a large and diverse array of pollination mechanisms to increase the chance of successful reproduction. Many plants can reproduce by self-pollination, cross-pollination, or clonal propagation. Depending upon a plant’s growth and flower form, different pollination vectors may be more effective. Those plants that are obligate out-crossers can be helped by any of three vectors (wind, water, or animal pollinators) and need not be restricted to one of them.
    Kearns and Inouye (1993: p. 45) state “[t]he structure of an inflorescence is likely to influence factors such as the foraging efficiency of flower visitors, the degree of outcrossing, and other aspects of plant reproductive success.” The family Araceae consists of 110 genera and over 2500 species distributed worldwide. Within this family there is a diverse array of inflorescence structures and pollination mechanisms. Some of the plants are very well studied, and their pollination mechanisms are well understood, as in the voodoo lily (Saurometum guttatum) and Italian lords and ladies (Arum italicum), which attract insects by odor and then promote mating behavior, or detain them overnight before showering them with pollen and releasing them (Bown 1988, Meeuse and Raskin 1988, Meeuse 1966). Other Araceae are poorly understood or simply unstudied.
    A number of tropical Araceae use heat and odor as attractants for their insect pollinators. Most often the heat is not the major attractant to pollinators; rather, it helps to volatize odiferous chemicals. Odors in the Araceae range from extremely putrid to delicately fragrant. The plants also tightly regulate the timing of odor release. For example, Philodendron bipinnatifidum has a gentle odor most of the time during its two-day flowering period, but between seven and nine at night it increases its temperature and therefore its odor output to attract scarab beetles (Erioscelis and Cyclocephala). Amorphophallus titanum is one of the more putrid of the Araceae. Its odor has been described by Sir Joseph Hooker “as a mixture of rotting flesh and burnt sugar” (Bown 1988: p. 39) Symplocarpus foetidus (L.) Salisb. ex Nutt uses heat to release a volatile amine, skatole compounds, and indole to create its rather fetid odors (Bown 1988).
    S. foetidus seems to require out-crossing (Meeuse 1966), but whether this is accomplished by wind, insects, or both is not definitively known. Out-crossing by water is unlikely, as the majority of inflorescences are not underwater even when they are growing in the middle of a stream. Several groups of insects, including Diptera (flies) and Hymenoptera (ants, bees, and wasps), have been suggested as potential pollinators (Kibota and Courtney 1991, Kevan 1989, Trelease 1879). It is also possible that the physical construction S. foetidus inflorescences facilitate wind pollination (Camazine and Niklas 1984).
    As little is known about the pollination mechanisms of S. foetidus, I have started with the question of whether wind and animals, especially insects, have an equal effect on its pollination success. First, it is critical to know whether pollen is actually available in the air and whether any pollen gathering insects are flying when the ovules are ripe. Non-pollen gathering insects could also be vectors if they use the inflorescences as heat sources, and in the process transfer pollen. If both insects and wind are important pollen transport vectors, the next question would be whether they are equally effective for successful fertilization.
 
Objectives and hypotheses of the project

    The main objectives of my eighteen-month study of Eastern Skunk Cabbage, S. foetidus, were to determine whether its reproductive success is pollen-limited, pollinator-limited, or controlled by other factors. To this end, I collected life history data on over 100 plants in a population of S. foetidus on the Mount Holyoke College campus during the spring and summer of 1999 and the spring of 2000. I also collected pollen and insects from 20 inflorescences during the spring of 2000. My experimental objective in the spring of 2000 was to determine whether there is an equal or unequal effect on pollen transport by wind and insects, and whether plant location has an effect on pollination. My three hypotheses are as follows:
H1. Wind pollination and invertebrate pollination have an equal effect on pollen transport between inflorescences in S. foetidus.
H2. Fruiting success percentages are no more due to pollination and fertilization success than to environmental factors such as soil moisture.
H3. Inflorescences are equally likely to contain external (non-self) pollen brought by wind as insect born external pollen.

Introduction to the plant, its structure and habitat.

          Natural History

    Symplocarpus spp. grow in damp woodlands and marshy areas of Eastern North America and Asia where winter water tables are at or near ground level. S. foetidus is one of the earliest flowers in the spring. It melts its way up through the snow to bloom using the heat from its cellular respiration (Knutson 1972, 1974, Meeuse 1966). In milder climates, such as Maryland, S. foetidus has been known to bloom as early as November, and as late as March. Further north, in Massachusetts, it starts blooming in February or early March. The leaves are bright green and appear after most flowering is finished and before most other plants have finished leafing out. At the end of the season, as the leaves start to yellow and senesce, the fruits begin to ripen, and a leaf bundle protected by a wintering over sheath may appear (Shull 1925).

            Inflorescences

    Skunk cabbage inflorescences have two separate interdependent parts: the spathe and spadix (Fig. 1). The spathe is the outer covering, which in S. foetidus looks something like a hood covering the spadix. The spadix is a quasi-spherical mass containing, on average, 65 flowers (Barabé 1993). S. foetidus appears to require cross-pollination to grow a multiple fruit that contains its seeds, and blooms in late winter, when few invertebrate pollinators are available.

Figure 1. S. foetidus plant with inflorescence. A. Spathe, B. Spadix, C. Leaf Bundle.

    The harsher the winter, the later S. foetidus blooms. Plants will only bloom once in a flowering season, although they can have up to four inflorescences depending on the health and strength of the individual plant (Shull 1925). The length of the flowering season is dependent on weather conditions, such as snow depth and temperature.
    The inflorescences of S. foetidus, and most Araceae, go through three distinct sexual phases: female, hermaphroditic, and male. Inside each spathe, flowers bloom from the bottom of the spadix to the top. The female portion of each flower comes into bloom first. After the stigma is done blooming, the anthers (male state) begin to bloom. Therefore a spadix can be all-female, hermaphroditic, or all-male. In the female state, just as the basal flowers begin to bloom, the spadix is gray and takes on a rather oily sheen. Then little golden droplets of odiferous liquid appear as each female flower blooms. When the flowers switch to the male state, these droplets are replaced by copious amounts of yellow pollen. This order of bloom makes self-pollination by gravity very difficult (Meeuse 1966). Self-pollination although not particularly successful does occur infrequently during the hermaphroditic blooming phase in S. renifolius (Uemura et al. (1983). In a wind tunnel experiment, Camazine and Niklas (1984) found that under specific controlled wind conditions, approximately 68% of the pollen within the inflorescence landed on the spadix. In a separate trial, 47% of the external pollen they released into the air encountered the inner surfaces of the spathe. This could possibly lead to self-pollination despite gravity.
    The physical construction of S. foetidus is also affected by its environment. Growing up through ice and snow requires unique adaptations such as self-thermoregulation (Knutson 1974). S. foetidus inflorescences heat themselves and regulate their own temperatures. The highest part of the heat cycle occurs when the female flowers are in full bloom. The plant actively respires in the spadix portion of the inflorescence (Knutson 1974). The heat is created by elevated and cyanide-resistant respiration (Knutson 1972). Cyanide-resistant respiration is an “alternative short branched” electron transport pathway that mainly produces heat instead of ATP, due to the lack of oxidative phosphorylation in the pathway (Lambers et al. 1998, Salisbury and Ross 1992). It is called cyanide-resistant or cyanide-insensitive due to the fact that this respiratory pathway can continue to function in the presence of cyanide. The presence of cyanide may not be necessary for this pathway to function, but as the Araceae are noted for the production of hydrocyanic acid (HCN), there may be a connection between the presence of such compounds and the plants’ control over heat (Lea and Leegood 1993, Meeuse and Raskin 1988). The heat from the spadix of S. foetidus diffuses the carbon dioxide and odors that are spontaneously produced during respiration.
    The precise purpose of heat production in S. foetidus is not known. Protecting the frost-sensitive spathe and spadix from freezing in sub 0° C temperatures is the most likely explanation, if there is one single explanation (Knutson 1972), but tropical Arums, such as the voodoo lily (Sauromatum venosum), also increase their respiratory rates and use the heat and odors to attract insect pollinators (Meeuse 1966). Knutson and Meeuse found S. foetidus inflorescences at 35° C above ambient air temperature, and its inflorescences regularly range from 15° to 35° C above air temperature (Knutson 1974). During sustained cold spells of -10°C and colder, inflorescence temperature may be kept just above freezing for a number of days. Longer cold spells cause the plants to sacrifice inflorescences to conserve plant energy (Seymour and Blaylock 1999). Other explanations for this heat phenomenon include heat aiding in the release of odors to attract insect pollinators, and heat aiding in the growth of pollen tubes or the inflorescence itself. The scents, released from the spadix, often mimic carrion or dung (Moodie 1976). Human tests show that S. foetidus inflorescences smell similar to garlic, apple, turnip and carrion (Kevan 1989). These odors may help attract insects (Moodie 1976). The heat itself may prove enticing for invertebrate pollinators. Whatever the purposes of self-heating are, the plant has a respiratory rate equivalent to that of a similarly sized small mammal (Knutson 1974).
    Pollination. The suggested pollinators of S. foetidus are wind, bees, and flies (Kibota and Courtney 1991, Kevan 1989, Camazine and Niklas 1984, Trelease 1879). The spathe, spadix, leaves, and fruit of S. renifolius, S. foetidus and Lysichiton americanum (a loosely related western North American member of the Araceae) provide good habitat for various fruit flies (Drosophila) (Kibota and Courtney 1991, Jaenike 1978). The habitat the plants provide, the fetid odors released by the inflorescence, and the reliance of its more tropical relatives on beetles and flies have led to the supposition that flies pollinate skunk cabbage.
Honeybees forage for pollen at S. foetidus inflorescences. Honeybees orient on the inflorescences, first by smell and then by sight. They use the coloration of the spathe to choose those spathes that have higher pollen content. Although the scents of S. foetidus vary from inflorescence to inflorescence, bees seem to pay attention only to the presence or absence of odor and visit odorless inflorescences statistically less frequently (Kevan 1989). Honeybees are unlikely to be the original primary pollinators of S. foetidus in North America as they often enter the inflorescence and gather pollen that has stuck to the inside of the spathe rather than investigating the spadix. S. foetidus did not coevolve with honeybees and therefore bees may have competitively excluded an original pollinator.
    Camazine and Niklas (1984) discovered that the asymmetry of the spathe opening sets up a “cyclonic vortex” in the space inside the spathe and around the spadix. The direction of the spathe opening did not influence internal airflow speed or direction. The ambient wind speed has little effect on the vortex speed within the spathe. This vortex creates an even temperature within the spathe. The airflow in the spathe directs pollen in a downward path allowing the pollen to adhere to spadix surfaces. The air currents within the spathe suck any pollen in the air near the inflorescence directly into the spathe and onto the spadix. The vortex may also serve to help release odors from the spadix.
    Leaves and Roots. Throughout its range, the plant is often evident during its inactive time of year as a small, pointed, green, tightly-packed leaf bundle that is covered by a “wintering over sheath” (Shull 1925). The leaf and inflorescence are rolled up inside this sheath. Leaf-rolling occurs in only one direction in small, young, pre-flowering plants. Older plants, those having bloomed at least once, roll their leaves in opposite directions to reduce friction on the inflorescence buds. This bundle of leaf and flower buds is often present from late summer until it begins to bloom or leaf out in the late fall or early spring. The leaves of S. foetidus expand out of the wintering over sheath after the spathe and spadix have begun to decay or begun maturing into a multiple fruit. The leaves are large, broad and a brilliant green and senesce in late summer.
    The bulk of the plant's mass is in the underground trunk. It is difficult to determine the actual age of an individual plant, as downward growth of the trunk compresses trunk material and friction removes it. Contractile lateral roots pull the plant down into the substrate to accommodate for saturated, shifting ground and frost heave making the plants difficult to uproot. These roots also aid in downward growth and plant survival (Bown 1988). S. foetidus clones itself from lateral growths off of the trunk. Lateral growths also provide insurance against destruction of the crown. If the crown is damaged, lateral shoots can grow into the flowering and photosynthetic portions of the plant.
    Fruit. The fruit consists of seeds embedded in the fleshy material of the spadix. All the flowers embedded in the spadix have the potential to mature into seeds. Multiple fruits appear in mid-summer to early fall. In studies of S. renifolius, all fruits were damaged by small mammal activity and 11% of reproductively active plants set seed (Wada and Uemura 1994). Multiple fruits are visible as and after the leaves senesce. The fruit is generally dark on the outside, although it can vary from a fairly bright green to dark brown. Fruit size ranges from the size of a cherry tomato to that of a large potato. The seeds inside are suggestive of groundnuts (Shull 1925) or pawpaw seeds.
 

METHODS

    Site Descriptions: Skunk cabbages, including S. foetidus, prefer habitats with high winter water tables; they therefore grow best around and in streams, seeps, vernal pools, and the marshy margins of larger fresh water bodies. My two sites were associated with small spring-fed streams and seeps near the large creek and the pond called Upper Lake on the Mount Holyoke College campus (Fig. 2). Both sites had similar species compositions comprised of: Trees, Acer rubrum (Red maple), Acer saccharum (Sugar maple), Quercus spp. (Oaks), Betula (Birches), Pinus strobus (White Pine), Picea (Spruce), Tsuga canadensis (Hemlock). Shrubs, Rosa (Roses), Diervilla lonicera (Bush Honeysuckle), Alnus (Alders). Herbaceous species, Impatiens capensis (Jewelweed), Osmunda cinnamomea (Cinnamon fern), Osmunda claytoniana (Interrupted fern), Pteridium aquilinum (Bracken fern), Arisaema triphyllum (Jack in the Pulpit). Nomenclature is after the Peterson guides to Eastern Forests (Kricher and Morrison 1988), Ferns (Cobb 1984), and Edible Plants (Peterson 1977), Audubon guides to North American Wildflowers (Niering and Olmstead 1995) and Trees (Little 1995), and Newcomb’s Wildflower Guide (Newcomb 1977).
    Site one consisted of three spring-fed streams that converged in a marshy area at the edge of the lake, and a small section of another stream. It was not continuous These streams remained wet throughout the summer despite the extremely dry conditions experienced by the entire area during the early summer of 1999. The streams used in site one are in predominantly southwest facing ravines and therefore tend to shed snow cover quickly compared with north facing slopes and ravines. The fourth stream section is somewhat more level and also receives a fair amount of sunshine. Site two was a roughly rectangular seep area further off in the woods beside Stony Brook. This site was partially under ice when I first delineated it, and became successively drier throughout the growing season.
 

Figure 2. Map of Mount Holyoke College campus with site locations.
Scale 1 inch = 1/2 mile (Courtesy MHC Earth and Environment
Department).
 

    Data Collection: In February 1999 I started studying a subset of reproductively active plants in the population of Eastern Skunk Cabbage, S. foetidus, on the Mount Holyoke College campus. I began by marking plants in site one and proceeded to add plants to both sites for approximately two weeks. I recorded the plant and inflorescence states on a weekly to bi-weekly basis. Plants were scored as to the state of their leaves, whether or not they had an inflorescence or fruit, and the state of that inflorescence or fruit. Inflorescence states were: not open (pre-flowering), open (in flower), past open (no longer flowering but not obviously decaying or fruiting), fruit, dead, completely gone, or ripe. Immature fruit were split between the past open category and the fruit category. I followed 136 plants, roughly divided into the two study sites. Sampling methods for the two plots were slightly different.
    In site one, to sample plants in the three converging streams, I walked up the middle of the streams marking inflorescence-bearing plants with flags as I encountered them. This site contained many more plants than I could follow, so I selected a set of 63 plants. These plants were mostly in the stream flows, as I was looking for plants with visible inflorescences when I started in early February 1999. Plants in the streams were more accessible to me than those on super-saturated stream banks or those covered by snow. My 63 plants in site one had a total of 94 inflorescences. Reproductively active plants represented approximately one-half to two-thirds of the population.
In site two I started by attempting to mark every plant within a rectangular plot, but it soon became clear that this site also contained many more plants than I could possibly census. I followed 73 plants with 132 inflorescences in site two. Both sites were followed in the spring of 2000 as well, although 18 plants from site one were no longer followed due to accessibility and non-researcher human disturbance. All life history data were examined for statistical differences between sites.
    Biomass: As the number of inflorescences may depend upon plant health and plant size (Shull 1925) it was necessary to attempt to measure plant biomass. I measured above-ground biomass by taking a set of 35 additional plants, some with fruit and some without, removing a leaf from each plant after measuring the leaf's length, width, thickness, and stalk length. I then measured leaf area ( + 0.1 cm2 ) with a Li-Cor leaf area meter, and dried it to a constant mass in a drying oven to get dry biomass. I took the same field measurements on 45 of my censused plants, measuring the size and state of all leaves.
    With the dry weight of the 35 leaves I had removed from my additional plants, and my field measurements of their length, width, and stalk length I created a regression using S Plus software. I then used the regression formula to generate approximate masses for the leaves I measured on 45 of my censused plants. The equation generated to predict leaf weight is as follows:    
   

 EQ1: PLM = 0.0077*L + 0.0175*W + 0.0054*SL

    Where PLM is predicated leaf mass in grams, L is length in millimeters, W is width in millimeters, and SL is stem length also in millimeters. Predicted masses were then used to determine an average above-ground biomass weight per plant based on number of leaves on an individual plant. Because leaf mass cannot be negative I forced this regression through the origin.
    Experiment on importance of annual green vegetative biomass: To test whether the removal of vegetation due to slug predation and senescence affects the survival and growth of fruit in the late summer, I conducted a leaf-removal experiment. I took a subset of 10 of the 35 plants from which I had removed leaves, and followed them from the date of leaf removal until mid-August, when I suspended plant censusing. I made observations of leaf and fruit state and attempted to measure the growth of fruits. Six of theses plants had immature fruit and four had no fruit. I recorded the same information for all of the plants I had been following since February 3, 1999.
Pollen collection experiments: This experiment was conducted in both study sites, with five replicates per treatment group within each site. I partially removed the spathe of each inflorescence, noted it is sexual sate and assigned it to a treatment group. Treatment groups were tanglefoot glue only, and duct tape and tanglefoot glue. Because spathe removal eventually results in desiccation of the inflorescences, the timetable of this experiment was fairly short: 65-72 hours. Spathe removal was intended to be partial to minimize inflorescence damage and the speed of desiccation. The sexual state of the inflorescences used for each was noted. Approximately half of the inflorescences in each part of the experiment were in the female state, the others were in the male state.
    The Tanglefoot glue treatment was designed to show which invertebrates were attracted to the inflorescence. I coated the spadix in Tanglefoot, replaced the spathe and left the plant alone. After 65-72 hours inflorescences were removed, frozen, and examined for insects and pollen that had been trapped. The duct tape and tanglefoot glue treatment was designed to collect the pollen that entered the inflorescence and to determine its mode of entry. In this part partial spathe removal procedure was the same, except that the spadix was wrapped in duct tape to minimize each experimental inflorescence's own pollen being caught in the Tanglefoot. The ten inflorescences from site two were caught out in a snowstorm during the latter part of the experiment.
    All insects found in the glued inflorescences were keyed out using Boror et al. (1976), and ANOVAs were preformed on the numerical data to explore statistical differences between insect assemblages due to variables such as location, treatment and plant sexual state. Due to the small numbers of insects analysis was at the order level.
 I placed sticky traps upright in the air column to look for windborne pollen and small insects. These sticky traps were left up for 4-1/2 weeks in site two and 3 weeks in site one and then examined for invertebrates and pollen.
    My next experiment lasted two weeks, with three sets of five inflorescences: one was hand-pollinated, one was left to its own devices, and one had limited or no contact with insect pollinators. The hand-pollinated set of plants was pollinated using pollen gathered from other inflorescences and dusted over the female flowers. Inflorescences that were left alone were manhandled in the same way as those that were hand pollinated. Covered inflorescences were manhandled and then covered with a paper bag to keep out insect pollinators. After two weeks all inflorescences were removed form the plants frozen and dissected. During dissection the inflorescences were rated for evidence of invertebrate damage, pollination, and rot. My basis for rating an inflorescence as pollinated was the swelling of ovules when the spadix was sectioned under the microscope.
 

RESULTS



    Life History: In 1999, I regularly surveyed 136 plants with 226 inflorescences. Of these plants 59, had only one inflorescence, 65 had two inflorescences, and 12 had three or more inflorescences. Forty-one percent of the flowering plants in site one had two or more inflorescences, as did seventy-four percent of flowering plants in site two. The number of plants per site was significantly different (P = 0.005), when split into categories by number of inflorescences on each plant, with a chi-squared value of 12.2 with two degrees of freedom. Site one had fewer inflorescences than site two.
    The inflorescences I followed were present as inflorescences from February 3, 1999 through May 4, 1999. In most cases, multiple inflorescences on a plant flower sequentially, after the first inflorescence reached the hermaphroditic state, other inflorescences on the plant began their blooming cycle. In the spring of 2000, I continued to follow 120 of these plants. They had 206 inflorescences by March 24, with forty-nine plants having one inflorescence, fifty-one having two, and thirteen having three or more each. Seven of these plants did not bloom in 2000. Two of these non-blooming plants were ones from which I had removed a leaf in July 1999. S. foetidus and many other plants flowered earlier in the spring of 2000 than in the spring of 1999. My data have an early flowing bias as I started selecting my plant in early February 1999 and quickly discovered that there were many more inflorescences in each site than I could possibly follow.
    Approximately forty of the 226 inflorescences that I followed in 1999 survived to some immature fruit state and fourteen of those became mature fruit. In site one, four plants successfully produced six mature fruit. In site two, eight plants successfully produced eight mature fruit. In site one 6.3% of the plants had mature fruit; the inflorescence to fruit success rate was 6.3% as well. In site two 10.9 % of plants had mature fruit but only 6% of inflorescences successfully became mature fruit. The number of fruit in each site was significantly different (P = 0.05) with a chi-squared value of 4.6 with one degree of freedom. 
    Pollen: S. foetidus pollen is large, monosulcate, and is textured (Fig. 3A). Grayum (1986) categorizes it as Foveolate/Reticulate. It is somewhat similar in size and shape to the insect-borne trisulcate pollen of Salix discolor (pussy willow) (Fig. 3C), and looks rather different from the local wind-borne pollen grains of Acer rubrum (red maple), and Corylus cornuta (beaked hazelnut) (Fig. 3 B and D) that appear around the end of S. foetidus’s blooming period. The other local member of the family Araceae, Arisaema has pollen categorized as Spinose (Grayum 1986).

 

Figure 3. Various pollen grains. A. S. foetidus, B. A. rubrum (Red Maple)(The small spots in the A. rubrum picture are the pollen; the large blob is a piece of the flower.), C. S. discolor (pussy willow) D. C. cornuta  (Beaked hazelnut). Scale bars are 10 micrometers.

 
 

    Biomass: Slugs were the only successful leaf predator observed during this study. They left large holes on leaves and often were found chewing on inflorescences and immature fruits. As slugs removed a fair amount of biomass, I considered the effects of potential biomass removal on plant health and fruit success. The regression line relating leaf size to leaf mass generated from my 35 cut leaves is shown in Figure 4. The equation for this line allowed me to generate predicted weights for leaves from my surveyed plants. The above-ground biomass in dry mass per plant grouped by number of measured leaves is shown in Figure 5. All mass values are in grams. Figure 6 shows box plots of individual leaf mass related to number of leaves on a plant. Leaves from plants with more leaves to be significantly larger (P= 3.78 X10--011 ANOVA), but the majority of leaves are within a similar dry mass range between four and thirteen grams (Fig. 6).

Figure 4. Regression line from the 35 cut leaf plants, forced though zero
 

Figure 5. Plant above ground dry mass approximation

Figure 6. Box plots of leaf mass by number of leaves on the plant.
 
    During late July and early August of 1999 and the spring of 2000, I followed ten of the plants from which I had removed leaves. The ability of these ten plants to set fruit 1999 or produce inflorescences in 2000 did not seem to be affected. Six of these ten plants had fruit and after leaf removal they retained their fruit until the fruit were ripe and removed by predators or the end of the survey. Eight of these plants produced inflorescences in the spring of 2000.
Inflorescence data: I observed a number of invertebrates in those inflorescences that I treated with glue. Of those invertebrates, potential pollinators were stone flies (Plecoptera) in the family Nemouridae. This family contains four sub-families, some that feed on cyanobacteria and some that feed on flowers (Borror et al. 1976). Honeybees (Hymenoptera) were observed in both study sites during both seasons. I did not find any honeybees in my sticky inflorescences, but I did observe them flying into inflorescences and gathering skunk cabbage pollen. Many families of flies (Diptera) are also common in both my sites and were present in my sticky glue-coated inflorescences. I also observed maggots in and on many inflorescences.
    In the inflorescences that I used to trap invertebrates, I found Isopods, Arachnids, and Insects. The members of the order Insecta in these inflorescences were Diptera (flies), Protura and Collembola (springtails), Thysanoptera (thrips), and Plecoptera (stone flies). In site one I had nine invertebrates; five Diptera, two Isopods, one Collembola and one Protura. In site two there were twenty-eight invertebrates in the ten inflorescences; six Diptera, eight Plecoptera, four Protura, five Collembola, two Thysanoptera, and one Arachnid, and two invertebrates that were too damaged to identify. The numbers of invertebrates found in the sticky inflorescences in each site were statistically different (P = 0.01, ANOVA). When invertebrate numbers were broken into family groupings some species were significantly different between the sites, others were not. The number of Diptera were not significantly different between sites (P = 0.67, ANOVA). There were still no significant differences when I separated the Diptera into families for analysis. The number of Plecoptera suggest a trend towards differences between sites (P = 0.06, ANOVA). Site one contained no stone flies in the glue-coated inflorescences.
    These inflorescences were also examined for the presence of pollen. Pollen was scored as self-pollen or non-self pollen. Self-pollen was from the inflorescences under examination and was in all male inflorescences in the experiment. Non-self pollen was pollen that came from another inflorescence, and so it was harder to determine its presence in an inflorescence. Only pollen that was obviously non-self was counted. Four of the female state inflorescences contained pollen. This pollen was non-self, as female state inflorescences have not started to create their own pollen. The presence of pollen was statistically significant (P = 0.00009 ANOVA) when compared to sex and not significant within female inflorescences (P = 0.54 ANOVA).

    Air column: The sticky cards that I had placed in the air column in both of my sites contained all of the invertebrates seen in the glue-coated inflorescences. Both sites had Plecoptera in the air column despite the fact that there were no Plecoptera in the inflorescences in site one. Both sites also had a number of invertebrates not found in the sticky inflorescences such as: honeybees, millipedes (Diplopoda), and many Diptera including Culicidae and Tachinidae. The cards in site one contained several Diptera not found on the cards in site two. These included Theveridae, Calliphoridae, and Simuliidae. The cards contained many invertebrate fragments that were unidentifiable.  

    Pollen experiment: Of the fifteen inflorescences in my hand pollination/pollinator restricted experiment, six showed some sign of successful pollination, five showed rot, and seven had invertebrates in them when I collected them from the field. Theses invertebrates were millipedes, maggots, adult flies, and one arachnid. The only factor that had any statistical influence on my observations of pollination was presence of invertebrates in the inflorescence (P = 0.02, ANOVA). Treatment type was not significant in this experiment. Those plants containing invertebrates showed significantly less evidence of pollination.

 

DISCUSSION

    S. foetidus plants are sensitive to annual temperature and moisture fluctuations. They survive slug and fly predation and successfully set fruit despite insects taking advantage of their pollen, eating immature fruit and leaves of all states, and, along with small mammals, gnawing on mature fruit and seeds  (Wada and Uemura 1994). These plants have a large number of fascinating adaptations, such as their thermoregulation and contractile roots, but they still seem to have a remarkably low fruit, and therefore seed, set. In this study, I attempted to figure out what factors affect pollination success and, secondarily, whether this success or failure of pollination and other factors affected fruit and seed set.
    One of my original hypotheses H1 was not supported by my numerical data or my observations. Evidence for the existence of wind pollination in S. foetidus was scarce in my observations. My attempt to test whether pollen was available in the air column provided no conclusive results. The sticky cards I placed in the air column caught many insects, so many, in fact, that it was imposable to tell weather or not there was pollen on the cards, and if so, whether it came off of an insect or whether it had been blowing though the air when it was trapped. Millipedes and other flightless invertebrates were present in and on inflorescences and sticky cards. They had access to the sticky cards in the air column, as the sticky cards were located at the same height as inflorescences. Several of the cards fell over so that they were lying flat on the ground. Cards were also often partially submerged in mud, streams or seeps consistent with positions of actual inflorescences.
    The hypothesis of wind pollination through the use of an intra-spathe cyclonic vortex as presented by Camazine and Niklas (1984) would be plausible if selfing of the plants was a practical option, or if pollen were actually available in a reasonable quantity in the air column. However, as selfing does not seem to be a particularly successful strategy for S. foetidus (Meeuse 1966) and I found no obvious way of getting pollen into the air column in reasonable quantities due to the physics of the internal cyclonic vortex, wind is an unlikely primary vector.
    Many insects, although not the ones most frequently cited as pollinators in the literature, are available in fair numbers during the flowering season, even in late January and early February. Stone flies emerge on snow-covered banks and other debris from the icy streams. Whether they are feeding on pollen or just seeking shelter from bad weather, they become coated in pollen when they enter an inflorescence. When cutting one inflorescence for my manipulative experiment with the glue I found a stone fly that was completely yellow with pollen in the inflorescence. Other insects tend to wait until later in the season when more of the inflorescences are in the male state and the weather is warmer. On a warm March day a myriad of Diptera can be found swarming around a patch of S. foetidus. Large numbers of honeybees will be swarming around the plants as well, flying in and out of spathes often without touching the spadix. Insect pollinators are available throughout the season but the actual successes of pollen transport by insects may be extremely low.
    My observations of the past year and the statistical trends shown by analysis of numbers of invertebrates caught in my glue experiment have led me to develop two new hypotheses:    H4. Stone Flies may be a major factor in early snowbound flower pollination. I suggest this because the stone flies I found in my sticky inflorescences were in the inflorescences in site two. The inflorescences in this experiment in site two were caught out in a snowstorm, whereas the inflorescences under the same experimental conditions in site one were not. Site differences may also play a factor in the insect distribution, although perceived differences in plant and insect behavior between sites may be due to the differences in sampling methods rather than to actual differences between the habitats.
    H5. Vegetation-feeding families of flies such as Drosophila may cause more inflorescence destruction than pollination by breeding in the spadices.
Drosophilid fruit flies are the most likely candidates for inflorescence and immature fruit destruction, as they have been documented breeding on and growing in the plants (Kibota and Courtney 1991, Jaenike 1978). Other vegetation-eating flies may find a safe and tasty haven in the plants as well, but the fact that several families are eating the plant does not exclude other Dipteran families from the pollination role.
    I observed honeybees foraging at many inflorescences. Often they would fly in and remove pollen, not from the flowers and spadix, but from the inside on the bottom and sides of the spathe. If an inflorescence has been manipulated in such a way as to change its odor the honeybees will not come near it. I observed one bee circling a glue-and-duct tape-treated inflorescence that was in the male state. It then proceeded to land on another male state inflorescence on the same plant. The bees' method of foraging for pollen is probably highly efficient for honeybees to collect the most pollen while reducing their risk of becoming trapped in the odd shape of the inflorescence. S. foetidus inflorescences are not bee flowers. Honeybees often get stuck in the inflorescences for minutes or hours, and sometimes never escape. Bees take advantage of the pollen as a food resource possibly more than they pollinate S. foetidus. Honeybees therefore may not be the most effective vectors of out crossing in S. foetidus even though they are foraging quite successfully in the inflorescences.
    Another factor that lends corroborative evidence for the insect pollination hypostasis is that of pollen morphology. S. foetidus pollen is large (Fig. 3) and is similar in size and shape to some of the other insect pollen in the vicinity. Grayum (1986) states that the other local aroid, Jack-in-the-pulpit (Arisaema), has spinose pollen transported by thrips and flies. Arisaema pollen is smaller as well as morphologically different. A comparison of Symplocarpus spp. pollen to the pollen of other Araceae with known pollination vectors might prove quite informative.
     I found very little obviously non-self pollen in my Tanglefoot treated inflorescences. This may have been due to the fact that I only put glue on the spadix, and that insects deterred by the odor of the glue may have avoided the inflorescences all together, or simply avoided the spadix. On several of my specimens I found a dusting of pollen towards the top inner part of the spathe. This dusting could have resulted from my flipping the spathe over and off of the spadix, or it could have represented wind-borne pollen that never made it down to the spadix, as my manipulative methods may have disrupted the flow of the cyclonic vortex. As the presence of pollen due only to sex had significance and male state inflorescences are almost defined by the presence of pollen, and as I could not tell self pollen from non-self pollen in the male state inflorescences, my data can not yet reject my third hypothesis.
    To address my second hypothesis I looked at the fruiting numbers within my sites and performed a manipulative experiment that involved hand pollination of a set of inflorescences. As there were no significant differences due to treatment in that experiment, this hypothesis is not rejected. However, as the presence of invertebrates was significant in facilitating decay in that experiment, the invertebrate biota may be having an effect on the fruiting success by eating some inflorescences that might otherwise mature into fruit. The significant number of invertebrates found in and on the inflorescences was probably due to the fact that the inflorescences and immature fruit had not been successfully or completely pollinated and therefore were decaying. Alternatively, the plants were rotting because invertebrates had visited them. A visit by an egg-laying Drosophila could indeed aid in the decay process and damage a pollinated inflorescence.
    The low numbers of actual fruit may represent pollination failure in my study. However, I cannot be sure whether this is due to some environmental factor during the duration of the study, the study area, or my sampling method. The differences between the sites suggest that soil water content, insect biota, or some other localized environmental factor may play a role. The behavior of the insect biota is a prime candidate for investigation when considering the question of low fruiting percentages. In the study by Wada and Uemura (1994) they saw eleven percent of reproductively viable plants setting fruit; this is higher than that obtained from either of my sites, although it is more comparable to the site two ten percent fruiting success rate. In studying the fruit success rate, it would be interesting to compare the fruiting ratios of Arisaema spp. and Symplocarpus spp., as the plants tend to grow is similar areas. If soil chemistry or other non-invertebrate environmental factors are playing a role in the fruiting success, this comparison may identify them.
    Bown (1988) and Meeuse (1966) have suggested beetles as predominant pollinators of S. foetidus, but as I did not encounter any beetles near, on, or in the inflorescences and plants I can only speculate on their importance in pollination. The lack of beetles may be due to location.
I did not investigate geographic relationships and nearest neighbor relationships between plants. Examining the factors relating to geographic location of the plants and their inflorescences might prove useful in determining whether differences between an inflorescence’s location changes its chances for pollination by wind or insects. Geographic location can also affect the foraging habits of honeybees and other potential pollinators.
    The questions relating to measurements of above-ground biomass and its effects on fruit and inflorescences require a longer-term project than could be encompassed in the scope of this study. Over a number of years, the appropriate data could be generated to see whether plant size may impact the number of inflorescences and be an indicator of plant health (Shull 1925). For this information to be useful in understanding the system and the influences of biomass on inflorescences and fruit, one would need to follow a set of plants for several years. From my observations and from statements in the literature by Shull (1925) and others it seems that the previous year’s biomass is more likely to affect this year’s growth than the current year’s biomass.
    My data support the hypotheses put forward by Knutson (1972, 1974, 1979), Meeuse (1966, 1988), and Seymour (1997), that odor and heat are potential attractants for invertebrate pollinators. My data do not support the ideas of Camazine and Niklas (1984) that wind is a major pollination vector; however, further study on wind pollination is necessary as the question of weather pollen is available in the air column still remains. Investigations of soil chemistry and invertebrate assemblages would also be useful in future examination of pollination mechanisms Symplocarpus spp., as the biomass and chemistry of different locations may be slightly different and have an effect on the pollination and fruiting success rates.
 
 
 

Acknowledgements

 
    I am grateful to my advisor Professor Aaron Ellison for his help, support, time and guidance in this endeavor and in all things academic and ecological, and to Stan Rachootin, Amy Frary, Ethan Temeles, Marian Rice, Mark McMenamin, Dianna McMenamin, Caroline Thorington and Richard Thorington for expert help, opinions and advice. I thank the Mount Holyoke College biology department, Mount Holyoke summer research fellowships, and Howard Hughes Medical Foundation for monetary support. Thanks also to my editors and scribes, friends and family without whom this would not be possible.
 

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