Abstract
Darwin’s analysis of the geomorphology of worms is the first documented account of fauna influencing the landscape and established the foundation upon which many current studies in ecosystem engineering, zoogeomorphology, soil science, and biogeomorphology are more broadly predicated. The focus of this assessment is to analyze the long-lasting and broad application of his 1881 work, The Formation of Vegetable Mould, Through the Action of Worms, with Observations on their Habits. In particular, this assessment identifies and elaborates on underlying lessons for today’s geomorphologists. The underlying lessons presented here are three-fold: (1) be multidisciplinary, (2) assess the trivial, and (3) be impactful. First, we review the context of geomorphology in his essay on worms. Then, we address each of the three underlying lessons. We discuss how geomorphologists have adopted these lessons, and what geomorphology can continue to learn from Darwin (1881). In doing so, we analyze the wide influence Darwin’s Worms has had on the scientific community, with an emphasis on geomorphic implications. Our analysis shows that over 900 publications refer to Darwin (1881). In addition, these publications were derived from a variety of disciplines including, but not limited to, anthropology, biogeography, botany, geology, paleontology, philosophy, psychology, scientific travel writing, taxonomy, and zoology. At first glance, it may appear trivial to assess the amount of earth moved by worms, yet this is how Darwin spent his final years. His efforts were not in vain, but rather found that worms play an essential role in soil health, and his work continues to gain recognition and inspire geomorphologists.
Introduction
The influence of Charles Darwin on the current scientific understanding of many subjects, including but not limited to anthropology, biogeography, botany, geology, paleontology, philosophy, psychology, scientific travel writing, taxonomy, and zoology, is monumental. Numerous assessments exist, which review the impact Darwin has had on modern science (Brown et al., 2003; Butt et al., 2008; Clark et al., 2009; Darlington, 1959; Feller et al., 2003; Kustchera and Elliott, 2010; Meysman et al., 2006), and abundant texts exist, which document the life history of Darwin (Bowlby, 1992; Browne, 1996, 2003; Clark, 1985; Darwin, 1888; Freeman, 1977; Gould, 1992; Holder, 1892). Despite these excellent reviews and life histories, many unstated lessons exist throughout Darwin’s work that are of value to geomorphology. The nature of this assessment, therefore, is to identify three unstated and underlying instructions for geomorphologists: (1) be multidisciplinary, (2) assess the trivial, and (3) be impactful. Although Darwin’s underlying lessons are applicable to all disciplines, they are particularly important to geomorphologists who regularly examine linkages among multiple interacting environmental systems. Darwin’s book, The Formation of Vegetable Mould, Through the Action of Worms, with Observations on their Habits (1881) (hereafter referred to as Darwin’s Worms) provides several excellent examples of Darwin’s unstated instructions and will provide the foundation for our approach. First, we review the content and organization of his essay on worms, highlighting the context of geomorphology. Then, we address each of the three underlying lessons. We discuss how geomorphologists have adopted these lessons, and what geomorphology can continue to learn from Darwin (1881). In doing so, we analyze the wide influence Darwin’s Worms has had on the scientific community, with an emphasis on geomorphic implications.
The geomorphology in Darwin’s worms
Darwin’s analysis of the geomorphology of worms is the first documented account of fauna influencing the landscape and established the foundation upon which many current studies in ecosystem engineering (Hastings et al., 2007; Jones et al., 1994), zoogeomorphology (see Butler, 1995; Hall and Lamont, 2003), soil science (Bhadauria and Saxena, 2010), and biogeomorphology (Viles, 1988) are more broadly predicated. Darwin’s Worms begins, as do many of today’s zoogeomorphic papers, with an assessment of the anatomy, senses, behavior, and habits of the organism under study. The physiology of earthworms segues to a discussion on the geomorphological aspects of earthworms. Darwin discusses his observations and measurements of the amount of earth that is brought to the surface by earthworms, describing the manner in which worms seize objects, their power of suction, and the tendency worms have to pile stones over burrows. The means by which worms excavate their burrows, the depth to which worms burrow, as well as the variations and stratifications in burrow linings, and the manner in which castings are ejected are all explained in unprecedented detail (Figure 1).
Images created by Darwin (1881) depicting the tower-like earthworm casting near Nice (left) and a casting from the Nilgiri Mountains in southern India (right).
Darwin also examines the impact worms have had in the burial of ancient buildings. Several articles published in Geoarchaeology have noted the contributions made by Darwin (Balek, 2002; Fowler et al., 2004). Johnson (2002) provided an excellent summary of this section, reviewing the details on how objects placed on the Earth’s surface become buried via worm action and examining how biomechanical processes failed to find visibility in early landscape evolution models. Reasons explored by Johnson (2002) included (1) a tradition in the Earth sciences of ignoring biomechanical processes and (2) a long time gap before a list of associated terminology emerged in the discipline (e.g. terms such as biomantle, bioturbation, biomechanical processes, faunalturbation, floralturbation, mollic epipedon, pedoturbation, stone-line, and textural differentiation).
The geographical denudation of the landscape is addressed in Darwin’s (1881) publication. Richards et al. (2011) indicated there has been little progress on the topic of net direction of soil flux since Darwin (1881). Darwin found that worms deposited almost two-thirds of excavated soil below the entrance of burrows and approximately one-third of the soil above the burrow entrance. For a listing of notable studies that report net direction of soil flux on burrowing activity of gophers in North America, examples of vegetation-related soil flux, and other downslope soil bioturbation, see Richards et al. (2011).
It is evident by the comprehensive content and meticulous attention to detail that Darwin’s book on worms is indicative of a ‘classic’ worth revisiting. Darwin’s Worms, however, is more than the mere sum of its parts. The remainder of this assessment focuses on several underlying lessons prevalent throughout the text that have potential to improve geomorphic endeavors.
Lessons from Darwin and his worms
Be multidisciplinary
Of Darwin’s many scientific contributions, his name is most commonly associated with his theory of evolution by natural selection (Darwin, 1859). His thoughts and writings on the process of evolution were revolutionary, and have influenced many scientific communities, including physical geography. Details on the geographical distribution of a diverse range of species, for example, can be considered pioneering work in biogeography. Research on the finches of South America and the Galapagos Islands were landmark contributions to the concept of island biogeography (MacArthur and Wilson, 1967). In geomorphology, and especially early American geomorphology, Darwin’s theory of evolution was the major influence behind William Morris Davis’s, Stages in the Fluvial Cycle of Erosion (1909). Davis applied Darwin’s concepts of biological evolution to the natural landscape, identifying a young, mature, and old sequence in the development of streams and landscapes.
Data were collected to analyze the array of disciplines Darwin (1881) influenced with his work on worms. Utilizing a combination of the Institute for Scientific Information (ISI)’s search data base, Web of Science, Ebsco’s Environmental Complete, Elsevier’s GeoRef, and Google Scholar, 936 unique scientific works that cite Darwin’s (1881) book were identified. A variety of data bases was necessary to maximize the number of unique cites (Harzing and van der Wal, 2008; Meho, 2007). This sample is not an exhaustive list; however, the 936 records do provide a representative sample of the academic disciplines citing Darwin’s final book. Search results revealed that citations of Darwin’s Worms were not limited to academic journals. Conference proceedings, theses and dissertations, professional meeting abstracts, and books all cited Darwin (1881). As one may expect, this work was cited across many disciplines. Articles came from over 400 different academic journals; of this list, several were selected at random and assessed to highlight the variety of influences made by Darwin’s work on worms.
In the context of sociology, the juxtaposition of the discreet function of earthworm bioturbation and the importance of soil turnover rates on agriculture was applied to human society (Graham and Thrift, 2007). In the social landscape of cities, the inconspicuous processes of infrastructure maintenance and repair often go unnoticed; however, these human activities are as essential to society as the bioturbation of earthworms is to landscape-scale soil turnover rates.
Darwin also had major influences in ecology. For example, an entomological study compared soil excavation of ground-nesting bees with Darwin’s Worms. Cane (2003) discussed Darwin’s calculated rates of soil erosion with interest in how it applied to the genesis and morphology of bee bioturbation. This study reported that the average weight of tumuli, or mound of excavated soil, was 26.3 ± 5.7 g (20–43 g). The total soil excavated by alkali bees was 4480 kg/ha, with an overall total of 87,500 kg of soil excavation.
Furthermore, Darwin’s application of worms has been applied to animal behavior. Liu et al. (2011) evaluated how Brazilian wild-bearded capuchin monkeys use tools to open nuts. Their study made reference to a variety of research on organisms and tool use and gave mention to Darwin’s observations on the earthworm’s ability to preferentially select different types of objects to fortify and conceal burrows.
An extension of worm intelligence into the discipline of psychology was addressed by Kono (2010), where he offered a new paradigm of intelligence referred to as an extended mind approach or ecological approach to humanized environments. This approach extends the idea of intelligence to include the brain, the body, and the environment. Kono (2010) recalled Darwin’s description of a worm’s perception of the external world characterized by their ability to choose types of leaves suitable for their burrows.
In addition to the diverse examples mentioned above, much geomorphic scholarship has noted Darwin’s study of earthworms. The introduction to the recently published special edition of Geomorphology emphasized zoogeomorphology and ecosystem engineering recognizing the zoogeomorphic work made by Charles Darwin (Butler and Sawyer, 2012). In the same issue, Meadows et al. (2012) and Eldridge et al. (2012) discussed Darwin’s influence in zoogeomorphology and ecosystem engineering. In their examination of biological modifiers of benthic macrofauna, Meadows et al. (2012) compared worm studies by Darwin (1881) and Davison (1891), who examined soil brought to the surface in intertidal zones by lugworms. Eldridge et al. (2012) examined the process of animal foraging and associated sediment movement and soil nutrient development in both semi-arid and arid regions in Australia. Their discussion of animal soil disturbance initiated with concepts from Darwin (1881).
The concept of ecosystem engineering originated with Darwin (1881). Jones et al. (1994) defined ecosystem engineers as organisms that modify, maintain, and/or create habitats. This process can either directly or indirectly affect the availability of resources for other species by altering biotic or abiotic materials. Wright and Jones (2006) revisited the progress, controversies, and future of the concept of ecosystem engineering. They recognized that, although, the term ecosystem engineers is relatively recent, it has long been acknowledged that organisms can impact geomorphological processes (Wright and Jones, 2006). Shortly after, the authors cited Darwin (1881) and his dedication of an entire book to the effect of earthworms on soil formation. Incorporating Darwinian evolution, Wright and Jones (2006) discussed the uncertain degree to which ecosystem engineering is a potent evolutionary force, that is to say, feedbacks in ecosystem engineering may lead to evolutionary consequences for the engineering species or for species affected by the habitat alterations.
Darwin’s work has been used as an example of early literature that acknowledged the influences between life and landscape (Reinhardt et al., 2010). This idea is contrary to the general direction of research throughout much of the 20th century, which emphasized spatial and temporal variations in physical processes affecting the distribution of organisms and biomass on Earth (i.e. constraints on where and to what extent life can exist). The well-known biogeographer, Arthur Tansley (1935) was also mentioned for similarly identifying biota affecting land-forming processes. Corenblit et al. (2008) offered geomorphic evolutionary insights, providing an extensive discussion and listing of historical research covering an array of connections between living organisms and landforms (i.e. ecosystem engineers, niche construction and changing, biogeomorphic inheritance and succession, and keystone species). Darwin (1881) revealed that bioturbation by worms could have significant effects on landscape dynamics and his work can be viewed as a foundational study of organisms changing their physical environment. Corenblit et al. (2008) also provided references for work that begins with Darwin (1881) (as well as Hutton, 1788), stressing the potential for organisms to impact large-scale geomorphology across land and ocean floor and highlighting the mutual interactions between landforms and organisms. Wilkinson et al. (2009) provided an excellent comparison of bioturbation measurements, location, climate, and methods used by Darwin, Shaler (1891), and more recent work in pedology.
These are but a small representation of how Darwin’s last publication has been used across disciplines and within geography. How has this study on earthworms branched out so vastly? Surely, his popularity from earlier studies on evolution had a major influence on the success of all of his publications, including his personal notebooks (e.g. Charles Darwin’s Notebooks from the Voyage of the Beagle; Chancellor and van Wyhe, 2009).
It is important to note that Darwin’s Worms was not purposefully multidisciplinary. Darwin was a natural scientist and as such, studied a subject by whatever means necessary to gain understanding. He was not bound by modern-day disciplines and paradigms. Modern-day research, however, is conducted by scientists trained in specific fields, typically without the broad training provided to natural scientists of Darwinian era. How can today’s geomorphologists learn from this lesson? Multidisciplinary work strengthens research and enables collaborative efforts by professionals throughout the scientific arena. Geomorphologists can be multidisciplinary by assessing the impact and application of our research on other disciplines. Biogeomorphology, phytogeomorphology, zoogeomorphology, and ecosystem engineering, subdisciplines of physical geography that trace linage to Darwin (1881), are all excellent examples of avenues for collaboration between disciplines of geography, ecology, geology, soil sciences, and ecology. In order to be truly multidisciplinary, geomorphologists are encouraged to work with other, non-geographers to establish conceptual linkages across traditional disciplinary boundaries. For example, a zoogeomorphologist may have a balanced understanding of the fauna and the geomorphic processes associated with the actions by said fauna; however, they may lack the intricacies of the fauna’s behaviors, details of habitat preference and tolerance, or the anatomy of the organism, all of which can be contributed by a biologist or ecologist.
Assess the trivial
Darwin referred to his book on worms as a ‘little’ book of ‘small importance’, which was of interest to himself, but not perhaps to other readers (Darwin, 1888). As is common in scientific endeavors, one does not know the extent to which a potentially trivial observation or publication may influence the advancement of scientific understanding. In an April 1881 letter to Victor Carus, Darwin wrote that he might have treated the subject of worms and vegetable mould in ‘foolish detail’ (Darwin, 1888).
Since the publication of Darwin’s book on earthworms, studies have burgeoned to include all aspects of earthworm ecology (see the edited volumes by Edwards, 1998; Edwards and Lofty, 1972; and Hendrix, 1995 for more information on biological, ecological, and distributional information of earthworms). Furthermore, many more recent studies on the zoogeomorphology of earthworms acknowledge and enhance Darwin’s assessment of the trivial (Anderson, 1988; Goudie, 1988; Hazelhoff et al., 1981; Henrot and Brussaard, 1997; James, 1991; Jouquet et al., 2008; Le Bayon and Binet, 1999, 2001; Schrader and Joschko, 1991). In Luxembourg, Hazelhoff et al. (1981) quantified the rate of earthworm cast production and determined that earthworms were responsible for the surficial deposition of 1.5 kg/m2 per yr of soil. In the tropics, the rate of earthworm cast production was found to be greater, with surficial deposit rates ranging from 2 to 30 kg soil/m2 per yr (Goudie, 1988). Henrot and Brussaard (1997) concluded that earthworms were capable of depositing between 260 and 570 kg/ha of casts annually. Their work also identified that cast production was episodic, with periods of high cast production followed by periods of low production. The broad distribution and variety of earthworms has resulted in certain scenarios where earthworms represent the highest individual contributor to overall soil biomass (James, 1991).
In addition to direct geomorphic effects of cast production, earthworms strongly influence the secondary geomorphic processes of infiltration, surface wash, rain-splash detachment, and soil creep. Anderson (1988) noted that earthworms were capable of producing up to 220 tunnel openings (ranging from 3 to 5 mm in diameter) per square meter, which increased soil infiltration rates (Goudie, 1988; Schrader and Joschko, 1991). Although surface wash tends to be the most logical method of cast removal, rain-splash detachment has been cited as the catalyst required to weather casts and prepare them for transport (Le Bayon and Binet, 1999). In fact, it has been suggested that the presence of earthworm casts retards surface wash because casts increase surface roughness and slow water flow (Jouquet et al., 2008; Le Bayon and Binet, 2001). The collection of work on worms as geomorphic agents has shown that the seemingly trivial processes of worm burrowing, consuming, and excreting, which function at fine scales, have impacts perceived at greater spatial and temporal scales and are capable of impacting multiple processes and systems.
Modern-day geomorphologists are well acquainted with the concept of scale. Schumm (1991) identified the potential problems associated with temporal and spatial scales when interpreting the Earth and suggested that the complexity of a subject increases with an increase in scale. Darwin examined fine-scale earthworm activity, which has proven to be influential at broader scales (James, 1991), but also noted burrowing processes and soil turnover rates at the landscape scale. Examining patterns and processes at multiple scales is not a new concept. However, it is interesting to note that research continues to emphasize the importance of examining processes at multiple scales (Meentemeyer, 1989; Schumm, 1991; Wu, 2004). Despite Darwin’s excellent example, articles highlighting the need for multiscalar work in geomorphology continue to appear and suggest that we are not adequately following Darwin’s unspoken lesson on assessing the trivial and applying the information at different scales.
An effective way for geomorphologists to implement this second lesson from Darwin is to identify relationships and make connections among phenomena, processes, and space across various scales. Many zoogeomorphic and ecosystem engineering studies have followed suite, detailing how the specific actions of fauna on a localized scale can extend to a broader scale. Most of these studies start with the small and work larger in scale; however, this does not always need to be the case. Imagine a scenario where a researcher discovers a cliff face covered in swallow mud-nests. This broad-scale observation may lead to research that identifies the localized surface disturbances where swallows gather the thousands of mud pellets needed to construct the nests.
Assessing the trivial was not a new concept developed by Charles Darwin; however, this seemingly trivial study remains a popularly cited text to this day. Darwin’s (1888) concern examining worms and vegetable mould in ‘foolish detail’ may now be seen as unwarranted, and yet, it is interesting to consider and reflect upon regarding our individual work. Darwin was able to transform a trivial study into something greater, a piece of literature that has inspired curiosity and further research on these small invertebrate organisms living out-of-sight, below our feet.
Be impactful
The success, and subsequent influence, of Darwin’s Worms was almost immediate among the general public (Brown et al., 2003). More than 6000 copies sold within the first year of publication and 13,000 copies sold by the end of the century (Freeman, 1977). Darwin’s Worms was the final scientific book produced by Darwin. Darwin had previously established himself as a well-known scientist with earlier publications, namely On the Origin of Species, and it is therefore not surprising that the text was widely read and highly influential. Furthermore, his treatise on worms was a re-visitation and compilation of his earlier pursuits in mould formation (Darwin, 1840) and individuals familiar with his work, would undoubtedly have found this volume on worms to be intriguing. Lastly, the death of Darwin, approximately 6 months after the publication of The Formation of Vegetable Mould, Through the Action of Worms, with Observations on their Habits, likely enhanced book sales and expanded his influence at the time.
To assess the impact Darwin’s Worms has had on scientific publishing, we examined results of a multi-database search of publication citing Darwin’s (1881) treatise (see section ‘Be multidisciplinary’). Unfortunately, several of the records identified in our search did not contain year of publication information. The sample size was subsequently reduced from 936 to 885 records. Figure 2 and Table 1 display decadal trends of citation for 885 scientific works that cite Darwin’s Worms. The data demonstrate relatively few citations of Darwin’s text until the 1980s, after which the citation rate doubled approximately every decade. Although the increase in citation appears impressive, it is not unique or uncharacteristic. Similar growth rates have been observed in many disciplines of academic publishing (Larsen and von Ins, 2010; Price, 1961). Furthermore, despite impressive book sales following publication, Darwin’s (1881) book was slow to be recognized and cited by the scientific community (Feller et al., 2003; Johnson, 2002). The latter part of the 20th century showed more citation of Darwin’s Worms (Figure 3), which may be attributed in part to the general increase in scientific publishing over time, advances in web-based searchable data bases, but more importantly, this increase coincides with advances and formal establishment of ecosystem engineering (see Jones et al., 1994), zoogeomorphology (see Butler, 1995), and other disciplines that recognize the importance of Darwin’s (1881) work.
What makes this work so impactful? Contemplating this question and applying it to our research is beneficial. Is measuring the number of times a publication is cited a viable way to determine its impact? To be clear, a lesson on being impactful does not suggest starting one’s research with the aims of obtaining a great number of citations and having influence on a variety of disciplines. Going beyond the sheer number of citations, being ‘impactful’ can, more suitably, be described as producing applied research that is beneficial to society and the environment, undertaking appropriate actions to disseminate our research, and actively seeking linkages between our work and that of others.
The number of times Darwin’s The Formation of Vegetable Mould, Through the Action of Worms, with Observations on their Habits has been cited between 1881 and the present. The text was cited 885 times during this time period.
The number of times Darwin’s The Formation of Vegetable Mould, Through the Action of Worms, with Observations on their Habits has been cited between 1980 and the present. The text was cited 754 times during this time period.
The number of times Darwin’s The Formation of Vegetable Mould, Through the Action of Worms, with Observations on their Habits has been cited between 1881 and the present. Citation information was obtained through Web of Science, Environmental Complete, GeoRef, and Google Scholar data bases.
Conclusions
We have attempted to glean unspoken insight from this classic Darwinian piece written more than 100 years ago. In an effort to better understand the long-term and widespread popularity of Darwin’s final publication, we identified three lessons for geomorphologists to consider. The first was to be multidisciplinary, which is especially desirable in the broadly applicable field of geography. The second was to assess the trivial. Identifying and studying seemingly trivial phenomena eventually led Darwin to a greater understanding of the impact of earthworms on the landscape. Geomorphologists are already cognizant of issues of scale. Continued efforts should be made to examine the impact of our work across scales to highlight the broader implications of seemingly trial research. The third and final lesson is to be impactful. With over 6000 copies sold within the first year of publication and 13,000 copies sold by the end of the 19th century, Darwin certainly made an impact with his publication on worms. Although these numbers are impressive for that time, impactful research is more than receiving high citations. An emphasis on cross-disciplinary work and contributing applicable research to society are perhaps more meaningful measures of impactful research. Likewise, we would like to encourage the continued efforts made in geomorphology to work collaboratively with other disciplines when possible. Creating linkages across disciplines strengthens research and brings together paralleled interests in the sciences. Utilizing the proper channels of dissemination will also lead geomorphologists toward impactful work. Presenting at multidisciplinary conferences and submitting research to journals that publish studies in various scientific fields will assist future collaborative and impactful efforts.
Although Darwin’s unspoken lessons should be practiced by all geomorphologists, it is often difficult to be multidisciplinary, spend time examining the trivial, and make an impactful contribution to scientific understanding. Demands on modern-day scientists, such as the pressures of teaching, obtaining tenure and promotion, service responsibilities, etcetera, do not afford scientists the luxury of time enjoyed by Darwin. Fortunately, Darwin’s unspoken lessons are complementary and, if properly executed, should enable geomorphologists to implement them in their work. A multidisciplinary approach to science requires scholars to examine the detail and have a solid understanding of their research at multiple scales. Only with a solid foundation in their cognate fields are scientists able to work with other disciplines. Furthermore, teams of scientists from multiple disciplines with extensive knowledge of processes across scales are able to produce research that is able to respond to challenging geographic inquiry and be applied in a way that is impactful for society and the scientific arena.
In closing, it is difficult to determine how well Darwin’s final book would have been received by the scientific community if his name and reputation were not as well recognized. Perhaps this ‘little’ book of ‘small importance’ would not have reached the multitude of academic disciplines it has to date, but then again, one does not know the extent to which a potentially trivial observation or publication may influence the advancement of scientific understanding.
Footnotes
Acknowledgements
The authors would like to thank the anonymous reviewers and David R. Butler for their insightful comments and suggestions.