Photo Gallery

Red-eyed Treefrog Metamorphs

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(Lower two pairs) Ecological character displacement such as that between omnivores and carnivores is only possible in ponds where both resources are abundant (upper left photo). In ponds in which detritus is rare (upper right photo), S. multiplicata is absent, and in ponds in which shrimp are rare (lower photos), S. bombifrons is absent. Thus, ecological character displacement, and therefore coexistence of close competitors, is only possible when diverse resources are available.

The sun sets along the road westward to Winton, in Australia’s northern rangelands. Like most rangelands, those in Australia are characterized by a high degree of resource variation, in both time and space. Before Europeans colonized these landscapes, seminomadic humans buffered resource variation through complex social institutions.

Pastoralism and private-property rights have since fragmented and disconnected Australian landscapes. But modern Australian pastoral systems are developing their own informal institutions, which are restoring rangeland connectivity over massive spatial scales.

A male Lark Bunting (Calamospiza melanocorys) is walking through vegetation after delivering food to his recently fledged young. Tracking radio-marked adults allowed us to track fledglings without radio transmitters.

        
Santa Monica Mountains National Recreation Area, Los Angeles County, California

Fuel break construction and maintenance methods can disturb soils and remove native plant cover, making fuel breaks susceptible to invasion by nonnative plants. Many fuel breaks have significantly higher cover, richness, and density of nonnative species than adjacent wildlands, particularly in areas that have been subject to recurrent fires or grazing.

 A marine iguana foraging in the low intertidal, Puerto Egas, Santiago Island.

The study shows that the outcome of plant–herbivore interactions on the diversity of rocky shore communities was drastically affected by changes in the in situ algal productivity (bottom-up effect) associated with the 1997–1998 El Niño and the posterior La Niña events, i.e., large-scale temporal fluctuations in temperature and nutrient levels. In non-El Niño years, herbivores tend to decrease the diversity of sessile organisms to a few grazing-resistant forms (top-down effects), but the El Niño impact on these consumers was subordinated to the local algal response to the spatiotemporal differences and fluctuations in the regional oceanographic conditions. These results provide new insight into the regulation of tropical rocky shores and the likely consequences of large-scale climate change on marine communities.

Introduction

The stability of natural ecosystems, including their resilience and resistance to perturbations, rests to a large degree on interactions and components of biotic communities (May 1973, 1974, De Angelis 1992, Holling 1996, Gunderson and Pritchard 2002, Ludwig et al. 2002). Interspecific interactions of communities, including, for example, the commonly studied predator–prey and competitive interactions, form the basis for ecological communities. Initial mathematical investigations into the stability of ecosystems revealed that interspecific interactions like those between predator and prey and competing species act to stabilize communities. In contrast, interspecific mutualistic interactions (those that benefit both interacting partner species through increases in per capita demographic rates of survival and/or reproduction [Holland 2002]) destabilize communities due to the inherent positive feedback associated with the interactions (May 1973, 1974). Initial mathematical models incorporating interspecific mutualism into communities, and analyzing for stability (May 1973, 1974), indicated that mutualisms must be unimportant and uncommon in nature, as they destabilize populations within the community. However, in nature, we know mutualism to be a common feature of natural communities worldwide, and empirical studies demonstrate that positive feedback associated with these interactions does not result in unbounded population growth (Heithaus et al. 1980, Thompson 1982, Roubik 1992:327–354). Thus, prior theory has not stood up to the empirical test. Despite our limited understanding of pairwise mutualistic interactions compared to pairwise predator–prey and competitive interactions, today these interactions are increasingly recognized as fundamental to the structure and dynamics of natural communities worldwide. Examples include pollinators and seed dispersers in tropical forests; nitrogen-fixing bacteria in deserts and agroecosystems; mycorrhizal fungi in grasslands; lichens in tundras; corals in marine systems; and microbes in deep-sea vents. Moreover, the ecosystem services mutualists provide are leading them to be increasingly considered a conservation priority (Buchman and Nabhan 1996, Costanza et al. 1997, Wall and Moore 1999).

There are two philosophically distinct classes of models that have been developed to address the effects of mutualist–nonmutualist interactions on community stability: (1) models whose predictions of community dynamics are sensitive to specific biological details about that community, and (2) models whose predictions of community dynamics are robust despite changes in the biological details of the system. Within each class of models are three ecologically distinct types of mathematical models: (a) population-dynamic models; (b) multispecies resource-based population dynamic models; and (c) multispecies spatiotemporal models.

The specific goals of this review are threefold. First, I present a brief history of the development of theory for exploring the population dynamics of interspecific mutualism. I then present theoretical approaches that are being used to address the effects of interactions between mutualists and exploiters on community stability. For each approach, I detail results and highlight models that have the potential to be operational in multiple empirical settings. This review can be thought of as preemptive: although the theory is in its infancy, there is a clear distinction between operational and nonoperational models. Without being too bold, I hope this paper leads theoreticians and empiricists toward models that are robust in their predictions, given only a general biological framework within which to work, as opposed to models whose predictions are only relevant for a specific set of a priori assumptions about the biological details of a specific system.

1. Theory development: the effects of intrinsic constraints on the stability of pairwise mutualistic interactions

Historically, mathematical analysis of communities has begun with mathematical models that explore the population dynamics of predator–prey and competitive interactions. The most commonly used models have been those that compare prey population dynamics in the presence or absence of a predator. For example, May (1973, 1974) used the classical continuous-time Lotka-Volterra ecological model (Lotka 1925, Volterra 1926) for n species (hereafter, Eq. 1) as a template for exploring the effect of changing the number of species in a predator–prey interaction on population dynamics. The model is described as follows:

             (1)

where N_i is the number of individuals, and R_i is the intrinsic rate of growth of species i. The parameter aij describes the negative density-dependent effect of species j on species i. The goal of such models is to track changes in species’ abundances over time. Predictions generated from these types of models are unrealistic, however, because they ignore nonlinearities in per capita growth rates, which when incorporated into the model, give rise to complicated system dynamics far from equilibrium (e.g., unbounded population growth).

May (1973, 1974) demonstrated that changes in the population dynamics of pairwise mutualistic interactions could be tracked by changing the sign in Eq. 1 from negative to positive. However, because this model relied on linear functional responses, positive feedback resulted in unbounded population growth of all populations, unless interaction coefficients were small, so that mutualism had little influence on interacting species. Numerous theoretical works have demonstrated that the interaction between two mutualist species can be stabilized by incorporating intrinsic constraints into Eq. 1. For example, the introduction of resource-handling times or metabolic costs incurred by one or both mutualists helps to stabilize the interaction (Vandermeer and Boucher 1978, May 1981, Addicott 1986). Recent mathematical models of population change in pairwise mutualistic interactions have shown that the benefits of mutualism that leads to positive feedback (i.e., saturation of benefits to per capita demographic rates of survival and/or reproduction) do not last forever. For example, by incorporating asymptotically or unimodal saturating functional responses into Model 1, Holland et al. (2002) were able to explain how mutualism has positive feedback, but not indefinitely. Specifically, their model showed that fundamental differences in population dynamics can occur when net effects to that population change linearly, unimodally, or in a saturating fashion.

2. Class 1 models

Multispecies population-dynamic models

Interestingly, mathematical models for exploring the population dynamics of mutualism in the presence of a third, nonmutualistic species are sparse, and have only recently started to grow in number. This can be attributed to two factors: (1) theoretical ecologists have only recently developed theory for understanding intrinsic mechanisms that stabilize pairwise mutualistic interactions, and (2) the introduction of a third nonmutualistic species into the basic Lotka-Volterra model for mutualism makes interpretation of qualitative dynamics and determination of stability criteria difficult . Although theory has been outpaced by empirical observation, models have been developed to explain the ecology of mutualism in a multispecies community context. Several studies have demonstrated that the incorporation of extrinsic constraints like a third species, either a predator or competitor, acts to dampen mutualist growth (Heithaus et al. 1980, Freedman and Rai 1987, 1988, Freedman et al. 1987). For example, Ringel et al. (1996) built a four-species community model by generalizing Eq. 1 to explore the effects of two additional species, a predator and prey, on the per capita growth of two mutualist species. The effects of each interaction type on the per capita growth of each population was either negative (self and predator effects), neutral (two species that did not interact), positive (prey and mutualism effects), or indeterminate (positive effects for mutualism, negative effects for nectar theft). Results of the model demonstrated that community interactions stabilized the four-species community. However, this type of model did not include intrinsic constraints on the inherent positive feedback between mutualists, which we know to be true in nature.

With this in mind, the model of Bacher and Fiedli (2002) is more appropriate for analyzing the dynamics of community stability because their model takes into account interspecific feedback between mutualists. The authors developed deterministic difference equation Lotka-Volterra models to ask the question: How was the well-studied mutualism between the shoot-base boring weevil Apion onopordi and the rust fungus Puccinia punctiformis influenced by the dynamics of their shared host plant Cirsium arvense, and vice versa (Watson and Keogh 1980, Thomas et al. 1994, Fiedli and Bacher 2001). In one version of the model, the rust pathogen was introduced into a thistle population that had reached carrying capacity, and the pathogen was then introduced into a thistle population well below carrying capacity. In the second version of the model, the authors allowed unbounded thistle population growth in order to evaluate the influence of host-plant dynamics on the qualitative dynamics of the three-species system. For both models, intrinsic constraints on the inherent positive feedback between mutualists included a trade-off in benefits of the mutualism for the weevil: ovipositing in infected shoots created an optimal food source for the first generation of offspring, but did not spread the rust, thereby leaving the second generation with an inadequate food supply. Growth of the weevil population increased when feeding on rust-infected plant tissue, which increased byproduct benefits received by the rust, which resulted in infection of healthy thistle in the year following weevil attack. The authors hypothesized that differences in the density of the weevil’s egg load between healthy and rust-infected thistles would regulate population abundances of the mutualists and their host plant. In contrast to the expected hypothesis, both models showed that the population dynamics of the mutualists were largely determined by the dynamics of their host plant. Analysis of the first model showed that neither the starting thistle population size nor its initial carrying capacity had an influence on the size of the thistle population at equilibrium. The second model demonstrated that changes in certain parameter values resulted in unbounded thistle population growth, which resulted in all three species either growing unbounded or going extinct. Hence, three-species coexistence was never reached, which led the authors to conclude that the mutualism between the weevil and the rust alone could not create or maintain system stability. In contrast, the population dynamics of the resource largely determined the stability of the host-plant mutualist.

Empirical evidence has demonstrated that exploiters of pollinating seed-parasite mutualisms are present in some communities (Kurdelhue et al. 2000, Pellmyr and Leebens-Mack 2000). Guided by these empirical findings, Morris et al. (2003) developed a mathematical model to explore conditions for stability of an obligate mutualism between a pollinating seed parasite and its plant host, and an exploiter (nonpollinating seed parasite) of the host. The parameters in their model were based on the general biological properties of a well-studied natural system consisting of flowering plants, pollinating seed parasites, and nonpollinating exploiters (Pellmyr and Huth 1994, Kurdelhue and Rasplus 1996, Pellmyr et al. 1996, Pellmyr and Lubens-Mack 2000, Marr et al. 2001). The goals of the model were twofold: (1) One goal was to explore how the rate of interaction between obligate plant-pollinating seed parasite mutualists and nonpollinating exploiters and the type of interspecific and intraspecific competition affected whether the exploiter could invade the plant–pollinator mutualism. (2) The authors also wanted to know whether three-species coexistence was stable. The model was based on the following simplifying assumptions: each fertilized ovule could support at most, one pollinator or one exploiter larva to pupation, and larval survival of exploiter and pollinating seed parasites was reduced by intraspecific competition when more then one egg was oviposited into a single ovule. Thus, the inherent positive feedback between mutualists was constrained by competition. Analysis of the model demonstrated that when competition among and between pollinators and exploiters was weak, the exploiter could invade and the three-species system could persist at a stable equilibrium. However, weak intraspecific competition resulted in a competitive advantage of pollinators over exploiters, which made invasion of the exploiter population and three-way coexistence impossible.

3. Class 2 models

Multispecies resource-based population dynamic models

Nearly all mutualisms, as is the case with predator–prey and competitive interactions, involve consumer–resource interactions (i.e., the exchange of nutrients between species [Holland et al. 2005]). The chemostat is both a laboratory apparatus and a theoretical construct that is used to investigate the ecological dynamics of consumer–resource interactions in continuous culture. The ecological dynamics of Eq. 1 can be examined within a theoretical chemostat environment, in which the effects of nutrient flow between species can be used to infer consequences of changes in population stability of pairwise predator–prey, competitive, and mutualistic interactions on the stability of communities.

In a theoretical chemostat environment, the culture vessel in which the species interact is mixed continuously, which results in a spatially homogenous distribution of nutrients, organisms, and byproducts. Thus, spatial interactions within the vessel can be neglected (Smith and Waltman 1995). Historically, classic continuous-time Lotka-Volterra differential equations have been the mathematical foundation for investigating interactions between predator–prey and competing species in a chemostat. However, the linear functional responses inherent in these equations give rise to unbounded solutions, whereby population sizes of interacting species grow indefinitely (May 1981, Murray 1989, Kot 2001). One solution to this problem is to include asymptotically saturating functional responses in the general Lotka-Volterra model. This allows the largely phenomenological Lotka-Volterra models to include mechanism. Such functional responses are useful because they render unbounded solutions impossible (Smith and Waltman 1995, Kooi et al. 2004) and allow for explicit modeling of nutrient flow through communities (Smith and Waltman 1995, Kooi et al. 2004). Surprisingly, only a limited number of studies have used the chemostat as a theoretical environment for exploring the effects of interactions between mutualists and exploiters on community stability. Kooi et al. (2004) developed a chemostat model of a well-mixed community of two mutualistic prey species with substitutable symbiosis coexisting on a single nutrient, and a predator population that consumed one (specialist) or both (generalist) prey populations. Both prey species were coprophagic mutualists (i.e., each species mutually benefited the other by feeding on the other’s waste products). The authors constrained the inherent positive feedback between mutualists by using a mass-balance model formulation. The model demonstrated that coexistence between a generalist predator feeding on two mutualist populations could only occur if exploitation of the mutualists by the prey was below a critical value. If exploitation was low enough, the predator was able to invade through the boundary equilibrium of two-mutualist coexistence. If exploitation was too great, the community collapsed and all species went extinct. Qualitative behavior of the dynamics of the model were robust to changes in intrinsic species parameters (e.g., intrinsic rate of growth, per capita death rate) and to parameters describing movement of waste products through the system.

Spatial–temporal models

The current trend in the theoretical study of the effects of mutualist-exploiter interactions on community stability is the use of simulation models incorporating spatial structure. The goal of these types of models is to understand how community stability is driven by the spatial distribution of populations. Empirical studies have demonstrated that there are interspecific mutualisms whose dynamics are regulated by their distribution among habitat patches (e.g., Thompson 1994, Yong et al. 1997, Yu and Davidson 1997, Parker 1999). Empirical studies have also demonstrated that attacks of mutualisms by exploiters in spatially heterogeneous environments can occur in a random pattern over a wide range of spatial scales (e.g., Hawkins and Compton 1992, Bronstein and Hossaert-McKey 1996, Yu et al. 2001). Wilson et al. (2003) used general biological properties derived from these empirical studies to develop an individual-based simulation model that incorporated stochastic interactions and spatial structure. Their model system was composed of two obligate mutualist species and an exploiter species of the mutualism. Like past models, the parameters in their model were based on the general biology of the well-studied interactions between a single species of plant, its pollinator insect, and an exploiter of the plant. However, their model was unique because it incorporated spatial heterogeneity in the distribution of the mutualist and exploiter species. The authors first constructed and analyzed a model of individual-scale interactions between the two obligate mutualist species and an exploiter species. Inherent feedback between mutualists was constrained by adding density-dependent effects in plant reproduction and by adding reduction in seed number as pollinator density became too high. Simulation results demonstrated that incorporation of spatial heterogeneity into the individual-based, nonspatial model resulted in the stable coexistence of all three populations. Analysis of the model demonstrated patterns of temporally constant, fixed-habitat patches. These patterns were robust to changes in the intrinsic parameters of mutualist and exploiter species (e.g., mutualist/exploiter density and life history traits).

Bronstein et al. (2003) used a spatial-stochastic simulation model with spatial heterogeneity to explore the population dynamics of obligate, species-specific mutualisms. They based their model on the general biological properties of the well-studied pollinating seed parasite exhibited by fig/fig wasp and yucca/yucca moth interactions (e.g., Dufay and Anstett 2003). Their model system consisted of plants and pollinating seed parasite insects in the presence of one of two obligate exploiter species: florivores or exploiter insects that parasitized seeds but failed to pollinate. Positive feedback inherent to the mutualism was constrained by extrinsic effects of exploitation, rather than the intrinsic effects generated by the mutualist interaction. Simulation results showed that mutualist populations could persist over ecological time in the presence of exploiter specialists, but temporal and spatial dynamics of the mutualist populations were altered in the presence of the exploiter. These patterns were robust to changes in the intrinsic parameters of exploiter species (e.g., exploiter density and life history traits).

Conclusions

This review has highlighted recent theoretical progress in exploring the effects of mutualist–exploiter interactions on community stability. There are two philosophically distinct classes of models for exploring these effects: (1) bottom-up or individual-case models that are constructed from the biological details of well-studied communities, and (2) top-down or system-based models that are constructed with limited a priori knowledge of the biology of the system. There are many weaknesses in individual case models, among them the fact that they are usually only operational in one particular biological setting, and the fact that their predictions are sensitive to changes in biological details. An additional weakness of the class 1 population dynamic models described in this paper is their use of simplifying assumptions about the biology of communities to make predictions of the model more tractable. This can result in spurious results, because these simplifying assumptions often do not match biological reality. For example, the assumption that only one ovule is produced per plant per season is unrealistic. Most importantly, unlike the predictions of class 1 models, which rely on the inductive method of hypothesis testing, the predications of class 2 models do not rely heavily on a priori knowledge of the biology of a system. Hence, class 2 models are robust in their predictions over a broad range of parameter space, and have the potential to be operational in multiple empirical settings.

Acknowledgments

Michael R. Golinski is supported by NSF grant DEB-0129630 to Dr. William J. Boecklen.

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Michael R. Golinski
Department of Biology
New Mexico State University
Las Cruces, New Mexico 88003 USA
(505) 646-5770
Fax: (505) 646-5665
E-mail: [email protected]

Scientists and academic institutions widely use Impact Factors ‹http://wos.mimas.ac.uk/› to evaluate the relative importance of journals. Although sometimes considered controversial, publishing in relatively high Impact Factor journals has been broadly applied as a stamp of approval for hiring and promotions, to rate the accomplishments of academic departments, and the importance of particular disciplines. Both authors and publishers strive to publish high impact journal articles, and the pressure to do so has apparently led to an insidious abuse in how some publishers correspond with authors of nearly accepted manuscripts. At or before the time of acceptance, several journals’ editors are requesting that authors cite additional papers published in that same journal. Some of these requests are general such as ‘We would also appreciate it if you would consider citing relevant past papers [from our journal] in your manuscript’, whereas others are more specific, with journal editors indicating one to several recent (often unpublished) citations.

Although the extent of this practice is unknown, at least four major journals in the area of ecology and evolutionary biology routinely encourage such self citation. Because Impact Factors are calculated by dividing the number of citations in the current year (e.g. in 2004) by the total number of articles published in the two previous years (i.e. in 2003 and 2002), citation of articles relatively hot off the press will increase the Impact Factor of a journal.

A gentle nudge by an editor to cite additional papers if relevant is all too easy to be uncritically accepted by most authors who are simply overjoyed with the news that their paper has been accepted. To maintain the integrity of objective scientific research, this questionable policy that essentially results in the ‘businessification’ of science must be stopped. Publishers should be embarrassed and authors should not comply.

[Reprinted from Trends in Ecology and Evolution, Volume 20, No. 4, Anurag A. Agrawal,
“Corruption of journal impact factors,” page 157, Copyright (2005), with permission from
Elsevier.]

Anurag A. Agrawal
Department of Ecology and Evolutionary Biology
Cornell University
Ithaca, NY 14853 USA

On 12 October 2005, the National Academy of Sciences of the United States of America released one of the most comprehensive looks at these concerns in a massive document called Rising above the Gathering Storm. The link to the executive summary is ‹http://www.nap.edu/execsumm_pdf/11463.pdf›, and the complete report can be found at ‹http://www.nap.edu/books/0309100399/html/1.html›. The blue ribbon committee that produced The Gathering Storm and the focus groups that assembled the in-depth information provide 10 recommendations.

Although The Gathering Storm is a United States document, probably many of the issues and suggestions are applicable in most countries. However, as ecologists, this document offers us another opportunity to remind the public and policy makers that the innovation that will drive the world’s economies in the 21st century will require considerably better understanding of the environment and ecology than has been true in the past. Some of the innovations in past centuries have created the environmental problems of today.

Rising above the Gathering Storm identifies two important challenges: creating high-quality jobs for Americans, and responding to the nation’s need for clean, affordable, and reliable energy. Certainly both of these challenges are not restricted to the United States; creating high-quality employment and finding environmentally and ecologically sound methods for producing energy to run our economies must be the goal of all countries. Again, ecologists might add to these two key characteristics, the fact that science and engineering must incorporate ecosystem services into their innovative developments. Together with the development of new energy sources, the addition of ecosystem services will be one of the biggest innovations since agriculture.

E. A. Johnson
Editor-in-Chief

There were five outstanding microscopists in the second half of the 1600s: Robert Hooke (1635–1703), Nehemiah Grew (1628–1711), Marcello Malpighi (1625–1694), Jan Swammerdam (1637–1680), and Antoni van Leeuwenhoek (1632–1723). All except Swammerdam had close ties to the Royal Society of London. Leeuwenhoek was the least educated but most persistent of them (Wilson 1995, Fournier 1996, Jardine 1999). The others published their findings during several decades, but by 1700 he was the only one still at it, and he continued this research until his death.

Leeuwenhoek’s father was a prosperous basket-maker in Delft who died when Antoni was six. In 1648 Antoni was apprenticed to a cloth merchant in Amsterdam. He returned home about 1654, married, and opened a shop to sell cloth, buttons, thread, and other goods.

He became a respected citizen and held several civic posts, and his close contacts included physicians and others better educated than he (Dobell 1932, Schierbeek 1959, Heniger 1973). His next-door neighbor was a physician, Cornelius ‘s Gravesande, who became the city’s anatomist; Leeuwenhoek began attending his dissections in 1668, and in 1681 when Cornelius de Man painted a group portrait entitled “The Anatomical Lesson,” he portrayed Leeuwenhoek standing behind ‘s Gravesande (Leeuwenhoek 1939–1999, III:Plate 1, van Berkel 1982:190–191).

Fig. 1. Antoni van Leeuwenhoek at middle age.

Leeuwenhoek saw a copy of Hooke’s Micrographia (1665) and—though he could not read the English text—became intrigued with the illustrations of microscopic investigations. He began making his own lenses and microscopes in 1673, and another Delft physician, Rainier de Graaf, wrote to the Royal Society of London (during the third Dutch–English war) on 28 April 1673 to inform its members that Leeuwenhoek made microscopes that excelled others available. His single-lens microscopes were more powerful than the double-lens ones then in use (Van Zuylen 1982). Along with de Graaf’s note were Leeuwenhoek’s first written observations, which the Society’s first secretary, a German living in London, Henry Oldenburg, translated into English and published in the Society’s Philosophical Transactions.

Fig. 2. Delft’s main street; in the distance is the tower of Old Church, where Leeuwenhoek is buried (Dobell 1932:Plate 4).

Leeuwenhoek’s first of several different observations were on mold on skin, flesh, and other things. In this he had been preceded by Hooke, who not only described mold as seen under his microscope in greater detail than Leeuwenhoek, but also illustrated it (Hooke 1665:125–127). Additionally, Leeuwenhoek described louse anatomy and several parts of bee anatomy (and provided illustrations of bee stings), both of which Hooke had also described and illustrated (Hooke 1665:163–165, 211–213). Hooke could have argued that Leeuwenhoek’s finds were redundant and therefore unworthy of publication, but instead the Royal Society not only published them, but also sent encouragement for him to continue his researches. With that encouragement he went on to become first of the founders of microbiology. All the other contemporary microscopists studied the microscopic structure of macroorganisms, as did Leeuwenhoek (Cole 1944:265–270), but he alone discovered the living world of microorganisms (Dobell 1932, Schierbeek 1959:58–79, Yount 1996). (Hooke’s discovery of fossil foraminifera shells and microspores of mold preceded Leeuwenhoek’s investigations [Bardell 1988, Egerton 2005a], but one may doubt that those discoveries made him a founder of microbiology.)

Fig. 4. Leeuwenhoek’s simple illustration of animalcules from frogs, which we call protozoa. A is Opalina dimidiate, B is Nyctotherus cordiformis, and C is perhaps a larval nematode. Drawn for the Dutch edition of his letter of 16 July 1683 (Dobell 1932:Plate 23).

Although Leeuwenhoek published letters in the Philosophical Transactions of the Royal Society of London for the rest of his life, the Philosophical Transactions did not always publish an entire letter, and it omitted publishing a few. Leeuwenhoek wrote some letters on a single topic, but most of them discussed several topics. Collected Dutch editions of his letters began to appear in 1684, and Latin editions in 1685 (Dobell 1932:390–397, Schierbeek 1959:205–209), which included letters that both did and did not appear in the Philosophical Transactions. About a century later, Samuel Hoole translated the published Dutch letters into English (1798–1807), but re-arranged them so that fragments of different letters on the same subject are grouped under topical headings; he did so without dating the fragments. He did provide an index, but no table of contents. Since his translation is reliable (Dobell 1950), I reprinted it in 1977, adding a brief introduction and bibliography. The various editions and translations constitute a bibliographic nightmare, but Francis J. Cole (1937) has provided an excellent guide, both to Leeuwenhoek’s publications and their contents. In 1939 a committee of Dutch scientists began publishing the definitive edition of Leeuwenhoek’s letters—with Dutch and English text on facing pages—and by 1999, 15 of the projected 19 volumes had appeared. Anyone having access to this set of large volumes can dispense with earlier editions for letters written by 1707, but those who lack access to it or wish to consult letters written after 1707 can use Cole’s guide with either Leeuwenhoek’s letters in the Philosophical Transactions or with Hoole’s translation, or both.

In a letter to Oldenberg, on 7 September 1674, Leeuwenhoek reported that he had gone to Berkelse Lake and placed some of its water under his microscope. He discovered at least three forms of life: green streaks in a spiral (now called Spirogyra, a green alga), and two kinds of animalcules—apparently what we call rotifers and Euglena viridis. In reporting his discovery of microorganisms, he encountered two problems that he could never handle very precisely: the naming of distinct species and their body parts. Leeuwenhoek was not a draftsman, and his brief verbal accounts aroused both curiosity and skepticism among members of the Royal Society. He hired a draftsman to illustrate his findings, and in 1683 published illustrations of protozoa (Fig. 4), which are of limited interest since the only details are their shapes.

Fig. 5. Leeuwenhoek’s Figs. 1–2: bdelloid rotifers (Philodina roseda), and Fig. 3, the protozoan ciliate Coleps (letter of 9 February 1702, originally published in 1702; reprinted from Leeuwenhoek 1939–1999, XIV:Plate II).

However, by the time he wrote his letter of 9 February 1702, in which he had the (“animalcule”) ciliate Coleps illustrated (Fig. 5), more details were drawn. He had also illustrated a rotifer (Fig. 8), and if not Spirogyra, at least the alga Volvox (Fig. 6).

On 14 June 1680, he reported his discovery of the incredibly small animalcules that we call bacteria; later he also had them drawn (Fig. 7). Since the bacteria came from a healthy person’s mouth, he did not think they caused disease. Some biologists have doubted that he could have seen bacteria; however, some of his microscopes still exist and have been used to show that he could have (Ford 1991).

Fig. 6. Now called Volvox, illustrating Leeuwenhoek’s letter of 2 January 1700 (Royal Society of London Philosophical Transactions 22:facing p. 483).

Fig. 7. Bacteria from a human mouth, letter of 17 September 1683. A is a motile Bacillus, B is Selenomonas sputigena, with C…D its path, E is Micrococci, F is Leptothrix buccalis, and G is a spirochaete, probably Spirochaeta buccalis (Dobell 1932:Plate 24 or Leeuwenhoek 1939–1999, IV:Plate 8).

Fig. 8. Duckweed from a Delft canal with associated animalcules, from Leeuwenhoek’s letter of 25 December 1702. The long structure in his Fig. 8 is part of a duckweed root, as seen under the microscope, with animalcules (rotifers, hydra, vorticellids) attached. For identifications, see Dobell 1932:277–278, Leeuwenhoek 1939–1999, XIV:Plate IX, or Ford 1982 (from Royal Society of London Philosophical Transactions 23:facing p. 1291).

Leeuwenhoek was an important experimenter (Meyer 1937)—a worthy successor of Redi—though by modern standards his experiments seem quite simple. For example, he discovered minute “vinegar eels” (Turbatrix aceti) in vinegar, and also several other kinds of microorganisms in pepper water (peppercorns submerged in water). Later he added one part of vinegar with “eels” to 10 parts of pepper water and found that all the animalcules in the pepper water died, but the vinegar eels continued to flourish (9 October 1676, Leeuwenhoek 1939–1999, II:125–129). As a merchant, Leeuwenhoek learned to note the size and quantity of goods, and he took this concern into his scientific studies. He developed fairly reliable methods of measurement. He compared the lengths of some microorganisms to the diameter of hairs on cheese mites. To calculate the number of microorganisms in a drop of water, he assumed that a drop of water is the size of a pea, and that a millet seed is 1/91 as large as a pea. He then drew into a pipette a quantity of water the size of a millet seed and divided that amount of water into 30 parts along the pipette, and estimated the animalcules in 1/30 of the water. Finally, he made the calculations to obtain the number in a volume of water the size of a pea. In this case, he estimated there were 2,730,000 animalcules (23 March 1677, Leeuwenhoek 1939–1999, II:119–201).

Leeuwenhoek never tired of making discoveries with his microscopes, but he also developed theoretical interests. One of the strongest such interests, which he constantly discussed, was the idea of spontaneous generation of life, against which he collected much evidence, beginning also with his letter of 9 October 1676. Dobell (1932:136, note 1) interpreted some comments in this letter as showing Leeuwenhoek debating with himself the possibility of spontaneous generation before he reached his firm opposition to the idea seen in his later letters, and Ruestow (1984) agreed. However, Leeuwenhoek’s modern editors think this is a misunderstanding of Leeuwenhoek’s less than crystal-clear comments (in Leeuwenhoek 1939–1999, II:101), and Smit (1982) appears to agree with these editors, since he does not discuss any ambivalence in this letter. The occasion for Leeuwenhoek raising the question of spontaneous generation was his discovery of microorganisms in rainwater that had stood in a cask for several days. A later example of Leeuwenhoek’s observations discrediting spontaneous generation is in a letter written 9 February 1702, stating that on the previous 25 August he had found animalcules (rotifers) in water from a house gutter, in which he observed that they became dry for a time, and then when wet again, their bodies swelled and they swam off.

He thought that if one did not know that they were dormant in the dry matter and then it became wet, one might think they arose spontaneously in the wet matter.

Another of Leeuwenhoek’s strong theoretical interests was in reproduction. This interest was sharpened by the discovery of spermatozoa (“animalcules” to him). A medical student, Johan Ham, told him in the summer of 1677 about his discovery of animalcules in the semen of a man with venereal disease; he believed they arose from the putrefaction of the semen. Leeuwenhoek refused to accept Ham’s idea on their origin, since that implied spontaneous generation. His study of his own semen (from his marriage bed, he informed the Royal Society) showed that spermatozoa are natural to semen. He reported his observations to the Royal Society in a letter written in November 1677, and in a subsequent letter of 18 March 1678 he included drawings of both human and dog sperm (Leeuwenhoek 1939–1999, II:280–293, 346–349, Plates 16–17). During his lifetime, he described sperm from 30 kinds of animals: 7 mammals, 2 birds, 1 amphibian, 7 fish, 11 arthropods, and 2 mollusks (Cole 1937:8). He soon concluded that sperm are embryos, and he rejected his townsman de Graaf’s conclusion that embryos arise after intercourse when eggs from mammalian ovaries enter the Fallopian tubes (Lindeboom 1982, Ruestow 1983). Leeuwenhoek thought ovaries are nonfunctioning in females, just as nipples are nonfunctioning in males. In a letter dated 13 June 1679, he rejected an Aristotelian report that mice reproduce by parthenogenesis (Leeuwenhoek 1939–1999, III:73–83), but in a long letter written on 10 July 1695, he reported (Leeuwenhoek 1939–1999, X:269–301) his discovery of parthenogenesis in aphids. He returned to this subject in subsequent letters (Cole 1930:90, 1937:224, Egerton 1967:6–16). After discovering parthenogenesis, he should have rethought his belief that embryos are contained in sperm. On other occasions he admitted his mistakes, but concerning parthenogenesis he went to extremes to avoid doing so (Cole 1937:12–13, Schierbeek 1959:105–106).

Still another of Leeuwenhoek’s persistent interests was in parasites. We saw in Parts 17 and 18 (Egerton 2005b, c) that this interest was fairly common among contemporary naturalists and physicians—focused on the natural history of parasites and interactions with hosts, without the parallel development of a theory of parasitology. In those days, most people had some first-hand knowledge of fleas and lice, and we have already seen that in his first letter to the Royal Society he had included observations on louse anatomy. He reported further on lice in a letter dated 15 February 1677, which is lost. In his letter of 5 October 1677, he reported observations on the development and metamorphosis of fleas. He had put several in a container and found that a flea can lay 15 or 16 eggs in 24 hours. He then carried enclosed eggs in his pocket and found they hatched in 8 or 9 days. He described the external anatomy of a larva and compared it to that of silk worms. He thought Swammerdam had mistaken flea droppings for eggs (Leeuwenhoek 1939–1999, II:245–253). Neither of these microscopists distinguished the different species of fleas they studied (Van Bronswijk 1982). In autumn Leeuwenhoek observed larvae spin cocoons, and a few days later he opened some cocoons and found inside weak fleas, which he thought were affected by the cold, indicating that they would not have come out by themselves until the winter ended (14 January 1678, Leeuwenhoek 1939–1999, II:319). On 12 November 1780, he sent observations on flea sperm (Leeuwenhoek 1939–1999, III:327). He reported further on flea anatomy and physiology in letters of 22 January 1683, and 15 and 27 October 1693. A goal of his flea studies was to determine the time period for each stage in the life cycle from egg to adult, which he finally achieved in his letter of 15 October 1693 (Leeuwenhoek 1939–1999, ?:211–227). He allowed fleas to suck blood from his hand in order to see the effect of food on egg laying.

In Holland, “gall-nuts” were imported from Aleppo, Syria for making dye. Leeuwenhoek assumed from the name that they were actually nuts, until he saw a local variety on oak trees and realized that they must be stimulated by an insect.

These galls were formed upon the large fibers, or vessels in the leaves, which were burst or broken, in the places where the galls were formed; so that I concluded that some insect had wounded or gnawed those vessels, and that the juices of the tree, flowing out of the wounded part, had extended themselves in globules and vessels, and thus, at length caused the formation of the gall-nut. [14 May 1686, Leeuwenhoek 1977, I:137]

He cut open some galls and found inside a living white worm. By continuing to open others periodically, he discovered that the worms became flies. He also studied “thistle-nuts,” which people carried in their pockets as health charms. He had a draftsman illustrate both kinds of galls and the associated insects (Fig. 9).

In 1700, fruit trees in Delft were infected with a great many flies, but when Leeuwenhoek examined them, he found they were associated with even more green lice (aphids), whose parthenogenesis he had discovered in 1695. The flies laid their eggs in the aphids, and later flies emerged from an aphid shell (Fig. 10).

He became interested in fish scales initially because Jews thought they could not eat eels and burbot, because each supposedly lacked scales and was therefore forbidden by Scripture. Using a microscope, he showed that they do have scales. When he examined an individual scale under a microscope he saw concentric dark lines, which he interpreted correctly as annual rings. The scale that he had drawn was thus seven years old (Fig. 12), and he assumed that this was also the eel’s age.

We now know, however, that eel scales only appear at age three, and therefore the eel would have been age 10 or 11 (Leeuwenhoek 1939–1999, IV:293–297, and note 48). Later, he attempted to determine the age of other fish, and an elephant’s tooth (Egerton 1967:9). When he turned to shellfish, he discovered that the layers of the shells were too numerous to be annual rings, and he speculated that they were laid down monthly, with the new moon (Palm 1982:159).

Leeuwenhoek lived almost 91 years and devoted the last 50 of them to science, primarily to biology, with an impressive number of his discoveries being on natural history, many of these on what we call ecological topics. His research and publications made him famous throughout Europe, and he was highly esteemed by leading scientists of the time.

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Acknowledgments

I thank Jean-Marc Drouin, Muséum National d’Histoire Naturelle, Paris, and Anne-Marie Drouin-Hans, Université de Bourgogne.

The Adirondack Ecological Center at Huntington Wildlife Forest, State University of New York College of Environmental Science and Forestry

The Adirondack Ecological Center (AEC) is a field station located on the Huntington Wildlife Forest (HWF), a 6,000-hectare experimental forest operated by the State University of New York College of Environmental Science and Forestry (ESF) in the geographic center of the Adirondack Mountains (see the map on right).

The Adirondack Mountain region is of national and global significance because it is a relatively intact natural ecosystem encompassing 2.5 million hectares and contains much of the remaining old-growth forest and wilderness in the eastern United States. Creation of the Adirondack Park in 1892 and subsequent state legislation brought about an unusual suite of regulations for public and private land that was designed to protect this ecosystem. However, the potential impacts of human activities on the region are immense. The Adirondack Mountains are threatened by development and pollution: the region is within a day’s drive of nearly one–third of the North American human population, and development is heavy along roadsides and lakeshores. The size of the region, diversity of ecological communities, natural resource-based economies and legal protection make this region an ongoing experiment in sustainability and therefore of vital interest to science and society.

In 1932, Archer and Anna Huntington established HWF for what was then the New York State College of Forestry at Syracuse now known as ESF (Fig. 2). HWF is located in the Town of Newcomb, Essex County and the Town of Long Lake, Hamilton County (44°00' N, 74°13' W). HWF was established specifically to provide an experimental site on which to investigate the central Adirondack ecosystem. The Adirondack Ecological Center (AEC) was established at HWF in 1971 with the intent of bringing more scientific expertise to the Adirondack Mountains and a long-range goal of broadening the impact of research and educational programming.

ESF has conducted research and educational programming at HWF for nearly 75 years. Data collected through monitoring and research projects are incorporated into the Adirondack Long-Term Ecological Monitoring Program (ALTEMP). ALTEMP provides an institutional framework for monitoring of over 100 physical, chemical and biological variables. Recognizing the value of these long-term datasets, HWF was chosen as a study site for the National Atmospheric Deposition Program (NADP), National Trends Network (NTN), Mercury Deposition Network (MDN), and Clean Air Status and Trends Network (CASTNET). AEC joined the Northeastern Ecosystem Research Cooperative (NERC), an initiative encouraging scientific collaboration in the U.S. and Canada, in 2000.

HWF operates year-round; all buildings have electric heat and light and some have kitchen facilities. Housing facilities in two areas on HWF currently accommodate up to 83 people during summer months. The Arbutus Lake Area contains researcher and graduate student housing and is often used for small classes and conferences. Several of these buildings were originally used by the Huntington family as a vacation home or “Adirondack Great Camp” (Fig. 3). They were built using plans of the famous Great Camp designer, William West Durant, and have significant historic character. Huntington Lodge has housing for 17 people, while other cabins in the area house 4-6 people each.

The AEC office building contains office space, a computer lab, conference room, library, and storage facilities. The lab includes computers, color and large-format printers, and high-speed internet access. Computers are networked and a wireless network allows roving laptops to connect throughout the building. The conference room is equipped with LCD projectors and a videoconferencing/distance learning system and is capable of seating 50 people. The AEC library holds approximately 1500 titles, including all graduate theses and dissertations relating to work on HWF, as well as technical and popular journals, textbooks, and other reference materials. The AEC library is integrated into the ESF/Syracuse University libraries, searchable via the Internet. The AEC maintains a Geographic Information System as well as a collection of about 500 museum specimens of birds and mammals for teaching purposes and an herbarium of 1,152 species that serves as a reference collection.

The Animal Studies Laboratory provides laboratory space, a wet lab, freezers, drying ovens, and cages for holding captive animals up to 20 kg in size. An outdoor pen complex for holding captive animals is also associated with this building. The Maintenance Garage contains workspace for carpentry and vehicle maintenance including a hydraulic lift. There are a variety of storage buildings throughout the property. HWF maintains snowmobiles, all terrain vehicles, 4-wheel drive trucks, and boats. A variety of field research equipment is available and includes animal traps, vegetation survey instruments, limnological and fisheries gear, and climatological and hydrologic devices. There are Trimble and Garmin GPS units available.

The research portion of HWF is gated and has 35 km of gravel roads; 3 km are plowed in winter and the rest are snowmobile-accessible. Approximately 400 ha area of old-growth forest occurs on HWF and was designated by action of the ESF College Trustees in 1941 as the Natural Area. The Natural Area serves as a control area for long-term studies. Of the seven lakes on HWF, Wolf Lake is rated as among the most pristine in the Adirondack region due to an assemblage of native aquatic species and limited influence by invasive species or human activities.

Staff at the AEC include a Director, Associate Director, administrative assistant, research support biologists, educational program coordinator, GIS specialist, forest properties staff, maintenance staff, and Dining Center staff. The Webb and Sage Apprenticeships are opportunities to provide a current undergraduate student or recent graduate with professional experience.  The apprentices gain experience by serving as a full member of the staff while developing skills in field biology, research, and leadership. Research assistants at the graduate and undergraduate levels are employed during summer.

Key attributes of HWF are its size and security. HWF offers the ability to conduct experimental manipulations on scales of tens to thousands of hectares. Approximately 85% of the 6,000 ha are behind locked gates accessible only by permission. HWF is large enough to accommodate experiments on areas of 10 to 2000 hectares and allow assessment of ecological effects across multiple spatial scales and forest types. In addition, agreements allow investigator access to adjacent state and private land parcels with different land-use histories. Many researchers use HWF as one of a network of sites to study ecosystem processes along a land use, forest age, or forest management gradient.

Research topics pursued at HWF are generally focused on ecology, hydrology, biogeochemistry, mammalogy, limnology, silviculture and wildlife management (Fig. 5). Two broad research areas encompass most of the research activity at HWF:

Integrated Forest Ecology and Management. Investigations focus on the dynamics of northern hardwood forest, alternatives for forest management, and the interaction of forest vegetation and vertebrate populations.

Biogeochemistry. Biogeochemical studies at HWF are part of regional and international networks and have an emphasis on forest ecosystems and freshwater. Research has included evaluations of atmospheric deposition, and investigations of the role of nitrogen and sulfur in soils and watersheds. These biogeochemistry studies have promoted cooperation among scientists in the U.S. and worldwide. Today, a multidisciplinary approach draws scientists at ESF, Cornell University, Institute of Ecosystem Studies, Kyoto University, Oregon State University, Syracuse University, United States Forest Service, United States Geological Survey, University of Calgary, and University of Waterloo. Studies at HWF are integrated with Hubbard Brook Experimental Forest in New Hampshire, Croton Watershed of New York, Bear Brook Watershed in Maine, Oneida Lake in New York, and Lake Erie research.

Among the most important research findings of recent years are the following:

Forest Dynamics: A series of studies dating back to the 1950s culminated in a new understanding of the interaction of herbivores, disease pathogens, site conditions and weather in shaping the species composition of northern hardwood forests. This work offers an alternative explanation to classic succession theory and gap-phase dynamics for the origin of the current overstory: the composition of the forest canopy persisting over centuries in this environment is shaped largely by episodic disturbance events occurring within a context of co-incident states of multiple ecological factors.

Social Structure in Vertebrate Populations: Intensive behavioral and genetic studies involving hundreds of deer on HWF over the past 30 years produced a new paradigm for the socio-spatial structure in northern deer populations. Deer have strong fidelity to a specific geographic area and social structure is based on groups of females. Research on HWF was instrumental in testing hypotheses about fidelity through experimental removal of a matrilineal group. The study has been replicated in other environments and the results are reshaping thinking about management of deer populations in parks and suburban landscapes.

Measuring Biotic Integrity: An issue of debate in the Adirondack Park has been how to measure the influence of human activity on the integrity of natural ecosystems. Research conducted through the AEC adapted the concept of biotic integrity from aquatic science to terrestrial environments. The index is built on breeding bird distributions across the region, and specifically, bird guild representation. Findings show that a relatively simple model incorporating landscape variables such as density of road networks can effectively predict changes in guild structure.

Biogeochemistry: Atmospheric deposition is an issue of concern throughout the eastern U.S. Research at HWF over the past 20 years has documented important changes in nitrogen and sulfur levels. A key finding is that movement of ions is more complex than originally hypothesized and highly dependent on not only local soil but also plants. For instance, the presence and role of nitrogen-fixing shrubs in wetland ecosystems are a critical regulating influence on the biogeochemical dynamics of nitrogen.

Forty-five research projects were conducted on HWF in 2004–2005. Between 100–125 faculty, agency scientists, graduate students and undergraduate research interns are active each year. Researchers are from ESF and other institutions including the State University of New York Colleges at Buffalo, Cortland and Potsdam; Columbia University; University of California-Davis; Cornell University; USGS; EPA; NOAA; US Bureau of Mines; and US Forest Service. Over the 70-plus year history of HWF, 500 refereed publications and 160 theses and dissertations have been completed. At the outset of an investigation, a Research Study Plan must be filed and approved. Summaries of current research are found at www.esf.edu/aec/research/currentresearch.htm. Data are stored in indexed file cabinets and on electronic media. An on-line publications list (www.esf.edu/aec/publications/publications.htm) is searchable by author and category. When permitted by publishers, abstracts are available on line.

Results of research at the AEC have fed directly into formal educational programs. Over 200 students took college courses in 2004–05, in courses such as Environmental Interpretation, Aquatic Entomology, Adirondack Forest Ecology and Management, Winter Mammalian Ecology, Forest Health, and Limnology & Fisheries (Fig. 6). Each year, HWF hosts numerous field trips with roughly 275 students attending from various academic institutions.

AEC also seeks to broaden the educational impact of Adirondack research through dissemination of scientific information to the general public. In 1990, AEC partnered with the state Adirondack Park Agency to build a Visitor’s Interpretive Center (VIC) on HWF. The VIC houses dioramas, classroom and office space, and an auditorium with a capacity of 150 people. Associated with the VIC are 4 km of trails with interpretive signs that introduce people to upland and lowland forest, wetland and lake communities. Each summer the AEC sponsors the Huntington Lecture Series at the VIC; the series attracts 350 visitors annually. In 1995, AEC partnered with the Town of Newcomb to upgrade an historic fire tower, construct a public parking area and trailhead on Goodnow Mountain, and create a kiosk and a series of interpretive educational booklets that expose visitors to research outcomes. The number of people accessing the VIC and the Goodnow Trailhead is over 25000 per year.

Visiting researchers and courses

Workshops, conferences, and short courses for professionals attract over 250 enrollees each year. For instance, each year 25 high-school biology teachers are exposed to current research methods and topics through Stalking Science Education in the Adirondack Mountains, an intensive weeklong course. The course focuses on the process of science and shows teachers how to use outdoor environments to excite students about science. An NSF-sponsored Chatauqua Short Course in Mammalian Ecology is offered to college science teachers in undergraduate education. Continuing education workshops in forest and wildlife management are geared toward natural resource professionals who wish to pursue certification.

In 2004–05, 7,200 user days were logged at HWF, including research, class and field trip use. With new facilities coming online, there will be more space for research and educational use of HWF. Visit HWF online at http://www.esf.edu/aec or for more information contact:

Dr. William F. Porter
Director, Adirondack Ecological Center
6312 State Route 28N
Newcomb, NY 12852
518-582-4551 voice
518-582-2181 fax
E-mail: [email protected]

Stacy McNulty
E-mail: [email protected]

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