Bryan B. Rasmussen, “Invertebrate Psychology before and after Darwin”


In his B Notebook on Transmutation (1837-38), Charles Darwin speculated that the “introduction of man” on the evolutionary scene was “nothing” compared to the insect, which he considered “the first thinking being.” More than any other class of life in the eighteenth and nineteenth centuries, insects and other invertebrates raised questions about the origins of mental experience and about the relationship between human and nonhuman nature. Their minds represented scientific insight at its limits, where traditional modes of observation and empirical experiment gave way to less certain tools of analogy and thought experiment. Darwin’s Origin of Species (1859) provides a useful historical touchstone for the evolution of these analogies and thought experiments, having constrained the field of plausible analogy from one that included physiology, philosophy, and theology, to the central analogy of common ancestry, or the shared evolutionary history of organisms. However, while Darwin’s theory of descent may have displaced other analogies, it did not replace them, and well into the late-nineteenth and early-twentieth centuries, invertebrate minds continued to inspire a variety of both novel and relic assumptions and methods for examining mental affinities with our spineless distant cousins.

I spend a lot of time around bees. I keep colonies of them where I work. I don’t know, but I’m fairly confident that my bees have personality. Maybe not each individual bee, but each colony. They have moods: sometimes they’re amiable and let me poke around inside the wooden skin of their hive with no trouble. Sometimes they’re not: like the time I had to sprint, in full bee-suit, to my car, jump in, close the door, and peel away, to lose 10 or 15 very angry members of that same hive. And I swear I’ve actually seen them think: once, a swarm of bees that split from one of our colonies had gathered on the branch of a guava tree in the campus garden. I saw them as a group, like it was one animal, quiver very subtly, all moving in unison like some gesture of assent. And within 90 seconds that swarm raised up in a huge cloud and flew off to find the new home that one of their members had identified as a nice place to live.

These behaviors would seem to express mind. If a colony of bees can appear to act rationally, can behave as if it possessed mind, isn’t that good enough to grant it one? Or maybe my assumptions about bee minds are little more than a common-sense manner of characterizing the behaviors of a complex system, for I am less sure about bees than I am about, say, my dog, another complex system, but whose familiar mammalian physiology permits behaviors that register more clearly as “mind-like.” Partly for reasons of shared physiology, and partly for less scientific ones, I concur with English metaphysician and dog-lover F.H. Bradley, who once wrote to the comparative psychologist C. Lloyd Morgan that “I never could see any difference at bottom between my dogs and me, though some of our ways were certainly a little different” (qtd. in Richards 105).

I begin with this little anecdote because it illustrates a common-sense method for thinking about the relationship between mind and behavior that philosophers of mind sometimes call the “intentional stance.” The intentional stance describes our assumption that the behaviors of complex systems express mental states such as intention, belief, and desire, and it is so embedded in our thinking, says Daniel Dennett, that “experimental psychologists of every school would have a hard time devising experimental situations to support their various theories without the help of their intentional expectations of how the test animals will respond to circumstances” (10). In other words, the expectation that the behaviors of complex systems imply mental processes akin to our own underwrites any scientific study of mind. Our common-sense models of mind are based on this stance, signaling our assumption that the world is possessed of mind like ours.

Evolutionary psychologists, of course, attribute such thinking about mind to the processes of selection. Employing folk models of mind aids in reproduction and survival. Just imagine if you could not attribute a mental state to someone leaning in for a kiss, or running at you with a knife. This essay will show, instead, that the sort of thinking that permits us to see in animals evidence of mind evolved over the nineteenth century. It investigates the role that insects and other invertebrates played in developing mental models for conceptualizing mind, and how this role changed over time. Insects, observes John F. Clark, represented to the nineteenth century the “minima of sentient beings” and therefore “an integral part of the search for […] the origins of life” (34). But as I’ll show, not just insects: invertebrates generally, whether bees and ants, or worms and jellyfish. And not only life, but mind—a quality that to some may have exceeded the boundaries even of biology. More than any other class of life, the invertebrates, organisms without a spine, raised questions about the origins of mental experience in nature, about the workings of natural selection, and about the quality of human experience. As such, they frequently could be found at the center of the most experimental sciences, forcing us to contend with organized life in its most alien forms, whose natures represented the very limits of our understanding.

This essay examines key works in the history of investigations into the brains and minds of these remote relations. I organize these explorations under the term “invertebrate psychology.” Invertebrate psychology wasn’t an actual discipline: its practitioners were interested in not only invertebrates, but a variety of natural world phenomena, from plants to polyps to people. Nevertheless, it does characterize a common willingness to explore scientific insight at its limits, where observation and empirical experiment give way to inference, analogy, and thought experiment. I am especially interested in the evolution of invertebrate analogies over the nineteenth century, and how these analogies helped natural historians investigate and characterize the limits of human and nonhuman animal affinities. How far “down” the chain of complexity, they wondered, do human and nonhuman animal affinities go? Do these affinities extend to mind and psychology? Where, and when, does mind begin? Is a comparative psychology possible?

The publication of Darwin’s theory of natural selection in 1859 provides a useful historical touchstone for thinking about not just evolution, but the evolution of analogy. The Origin of Species changed the frame, so to speak, of examinations of invertebrate behavior and mind by constraining the field of plausible analogy, from one that included the theological, philosophical, and physiological, to one that placed common ancestry, or the shared evolutionary history of organisms, at the center. It wasn’t that Darwin’s theory of common ancestry simply replaced theological or philosophical invertebrate analogies: rather, that these analogies now had to be framed by the question of common ancestry. Theology and philosophy may no longer have provided the central frame, but they continued to inflect, in both obvious and less obvious ways, the science. Nevertheless, this constraining of analogy did not lead to an overall uniformity in approach to the investigation of invertebrates. If anything, it led to a flourishing of approaches and methods.

The central artifacts in this discussion are a series of representative experiments that provided their respective naturalists with the raw material for analogy. These experiments may have been empirical experiments in the physiology and behavior of invertebrates, or thought experiments in method. Sometimes the line isn’t clear. I highlight the work of four scientists between about 1830 and 1930: Darwin himself, the Victorian pioneer of evolutionary psychology who sought the evidence of “the first thinking being” in the lowly earthworm (Darwin, B Notebook 222-23; B207-08); George Romanes, Darwin’s protégé on the question of mind, who aimed to provide the physiological and philosophical conditions for the study of mind; Jean-Henri Fabre, the French entomologist who modeled a psychology without evolution from the wonderful instincts of insects; and August Forel, the Swiss neuroscientist and naturalist who found common ground between his psychiatry and his myrmecology, or the study of ants.

First, though, I provide a historical context for understanding the nature and implications of these experiments, beginning in the eighteenth century with debates about the relationship between instinct and intelligence, where invertebrate psychology first began. I’ll briefly examine some influential thinkers in these debates: from René Descartes and Antoine Réaumur, to Erasmus Darwin and William Kirby and William Spence.

Though I range fairly broadly, this cannot claim to be a comprehensive analysis. I have for the most part limited my attention to those writers that didn’t simply characterize insects and other invertebrates but who put our spineless distant cousins to use in answering methodological questions about how we can know the natural world. As such, invertebrate minds provide a key to some of the contemporary challenges of imagining connectedness with nonhuman nature, and so in my conclusion I will briefly discuss echoes of the nineteenth century in the late twentieth. Nevertheless, despite the diversity of assumptions and approaches exhibited here, many of these thinkers shared a common desire to find the familiar in perhaps the most unfamiliar place on earth: inside the minds of invertebrates.

Brief Philosophical History of Comparative Psychology

It’s difficult to overestimate the influence of—and many would argue, the damage done by—the seventeenth-century French philosopher René Descartes on the study of animal psychology. Descartes introduced two ideas into Western philosophy that are material here: first, that mind and body are not the same (philosophers call this dualism). For Descartes, mind is not matter. It is immaterial. Second, that animals are machines. Descartes drew a sharp line between us and the animals. To him, “animals mimicked intelligent action” (Richards 22), but possessed no will, no mental activity, and thus no psychology. Among the first to criticize Descartes was the eighteenth-century French sensationalist philosopher Étienne Condillac (1714-80). Sensationalists identified the origins of the complex behaviors of animals in the physiology of the senses. For them, “all human faculties and all human knowledge are merely transformed sensation” (Fabre, Wonders 43, trans. note). Condillac believed that even just one sense, smell, was alone a sufficient minimum for mind. In a famous thought experiment, Condillac “imagines a statue, organized like a man, and endows it with the senses one by one, beginning with […] smell” in order to determine sense criteria for mind. Smell alone, he thought, could produce memories that might develop into ideational associations and even imagination—that is, the stuff of mind. In this way, Condillac connected mind and body where Descartes had cleaved them, proposing even that “supposedly blind instincts” were in fact “intelligently acquired habits” (Richards 25). With this relationship between instinct and intelligence, Condillac opened the door to a comparative animal psychology.

Antoine Réaumur and the Origins of Invertebrate Psychology

Invertebrates got their first real advocate in the eighteenth-century French entomologist Antoine Réaumur (1683-1757), who was among the first to demonstrate, through experimentation, that insects possessed a psychology by analogizing from their behaviors. The Victorian biologist T.H. Huxley considered Réaumur the Darwin of insects: he said that he “knew of no one [else] to be placed in the same rank” with Darwin for the detail and acumen of his experimental science (qtd. in Wheeler 5). In his monumental six-volume work, Memoirs of the Natural History of Insects (1734–1742), Réaumur’s attention to the variety and complexity of insect behavior led to an examination of the “inner faculties” of insects (32). We might date the invention of invertebrate psychology—even the science of ethology, or animal behavior, as Morton Wheeler claims—to Réaumur’s examination of these inner faculties (36). So complex and varied are the behaviors of insects that Réaumur saw in them the order of life itself. He went so far as to classify them not according to their structure, or morphology, but according to their “industries,” an eighteenth-century French idiom for “behavior” (28).

Réaumur was a near contemporary of the Swedish naturalist Carl Linnaeus, to whom we credit, among other things, the discovery of the science of taxonomy based on a comparative anatomy. Comparative anatomy is the study of the morphology, or the form and structure, of living things. Comparative anatomy gave scientists a ready method for taxonomizing life, for classifying things in order to draw inferences about their relationships. Until fairly recently, with the advent of gene-level comparisons, the classification of organisms based on form and structure had been the basis of modern life sciences. Linnaeus chose the sex characteristics of plants as his standard, a largely arbitrary choice, but which was easy to use and allowed for the first wave of citizen scientists to contribute to the ordering of life.

But as Linnaeus’s critics noted,[1] there is an infinite number of classifying systems on which to base a science of life and structural comparison is just one. Réaumur’s appreciation for the multitude of insect behaviors suggested to him another, equally valid system. Within his class of insects Réaumur included not only some non-insects like “worms, polyps, mollusks, arachnids, myriapods and crustaceans” (Wheeler 29), but also the reptiles, saying “‘[t]he crocodile is certainly a fierce insect, but I am not in the least disturbed about calling it one’” (qtd. in Wheeler 29). “The crocodile was to him an insect, because it behaved precisely like a huge, predacious, amphibious insect, and the honey-bee, caddis-fly, and ant-lion were more interesting than forms like Amphioxus, Balanglossus and Peripatus because their activities made a much more direct and intelligible appeal to the human observer” (Wheeler 30, emphasis added). Classification based on behavior seemed to Réaumur a more natural taxonomic system because on this basis our relationships with other creatures seemed common-sensical. Two creatures that shared few if any anatomical similarities might nevertheless behave the same. To Réaumur, the behaviors of honeybees and the like suggested analogies to human behaviors, and based on these analogies Réaumur granted them an inner life, a psychology. Furthermore, through shared behavior they might even suggest a comparative psychology.

But Réaumur was sensitive to the idea that insect psychology could be a victim of philosophical prejudice. In his Memoirs Réaumur writes:

[S]hall we refuse [them] all intelligence?” he wonders. “Shall we reduce them to the simple status of machines? […] We behold in […] insects […] processes which incline us to assume a certain degree of intelligence. We are led to take this view by reasoning from analogy. But the insects are reproached with having processes that are too uniform; they do not exhibit sufficiently varied activities […]. But even if the insects performed actions more surprising and more varied […], like our own, they would yet gain nothing in the estimation of those who are determined to refuse them souls. (qtd. in Wheeler 34)

Réaumur points to a philosophical problem in comparative psychology that persists even today: Namely, that whether we think nonhuman animals possess mind—and thus soul—depends on whether or not we think making common-sense analogies is a valid scientific pursuit. For if insects exhibit complex behaviors with human analogues, then only a Cartesian would deny them an inner life. The figures in the rest of this analysis tend to fall along one side or the other of this conundrum.

Erasmus Darwin’s Romantic Insects

The philosophical coup for an invertebrate psychology came at the end of the eighteenth century, in Charles Darwin’s grandfather Erasmus Darwin’s 1794 work Zoonomia, or the Laws of Organic Life. Darwin, like Condillac, was a sensationalist: he philosophized that all mental faculties were attributable to input from our physiological senses—touch, smell, vision, and the like. He would use this physiological comparison to locate a psychological common denominator in humans and invertebrates. Despite what he calls our “very imperfect acquaintance with the various tribes of insects” and the obvious differences in “their occupations, manner of life, and even the number of their senses,” “there is,” he says, nevertheless “reason to imagine, that those which possess the sense of touch in the most exquisite degree […] are indued with a greater portion of knowledge and ingenuity” (175-76). “Ingenuity,” like “industry” for Réaumur, was Darwin’s byword for “behavior.”

Armed with this base-line comparison, Darwin analogized freely. In one example, he finds evidence of reason in the spider’s ingenious web—or “net” —building instinct:

The production of these nets is indeed part of the nature or conformation of the animal […]. [W]hen she employs them to entangle her prey, there are marks of evident design, for she adapts the form of each net to its situation, and strengthens those lines, that require it, by joining others to the middle of them, and attaching those others to distant objects, with the same individual art, that is used by mankind in supporting the masts and extending the sails of ships. (176)

If instinct can produce behavior analogous to intelligence—as in ship-building—then human and animal ingenuity existed on a continuum, and instinct and intellect were in fact comparable. From the emotive force of such analogies, Darwin ascended to a crescendo of appreciation for the mental powers of insects: “If these are not deductions from their own previous experience or observation, all the actions of mankind must be resolved into instinct” (181). And it was this paean to animal intelligence that introduced the nineteenth century: “Go, thou sluggard, learn the arts and industry from the bee, and from the ant! Go, proud reasoner, and call the worm thy sister!” (183).

Deus Ex Insecta

Erasmus Darwin had an inkling that instincts emerged from the life history of the animal—that they were part of the individual’s development, acquired through “observation” and “tradition.” Thus while mysterious, instincts nevertheless were possessed of the same physiology that produced reason. He was also an evolutionist—he believed that more complex organisms derived from simpler ones. Against both these premises were the natural theologians of the nineteenth century, for whom invertebrate minds provided powerful analogies, not with human minds, but with the mind of God. They aimed to connect scientific insight with theology at the lowest, most minute levels of the natural world.

For this reason, argues Clark, entomologists remained strong proponents of special creation and among the last to accept natural selection (109; 111). What we might call the “argument from instinct” understood invertebrate instincts as confirmation, not of the origins of intelligence, but of the divine perfection of nature. To natural theologians like William Paley, instinct was “‘a propensity, prior to experience, and independent of instruction’, which resided in the Creator” (qtd. in Clark 36). Instincts were “perfect” and perfectly regular across species. “Plastic” reason, on the other hand, according to Paley, was the exclusive domain of man. Reason was the basis of choice and free will, for without reason, imperfect human nature could neither benefit from moral instruction nor seek perfection under God. Paley’s natural theology did little to challenge the prejudice against invertebrates that rendered them mere machines, except to make the machine an analogy for the mind of God. In his Natural Theology (1802) Paley’s most famous analogy merely confirmed this: watch is to nature as watchmaker is to God, an analogy that was as applicable to instincts as it was to eyeballs.

But actual observers of insect behaviors evolved more sophisticated divine analogies that came closer to psychological insight. William Kirby and William Spence, in their influential Introduction to Entomology (1818-1826), followed Paley in pressing their study of insects into the service of a natural theology that viewed God as the ultimate end of the study of the natural world. Of the branches of natural history, they wrote, “[n]o study affords a fairer opportunity of leading the young mind by a natural and pleasing path to the great truths of Religion, and of impressing it with the most lively ideas of the power, wisdom, and goodness of the Creator” (1: xvi), than entomology. Like Paley, they maintained a firm distinction between intelligence and instinct. Of those doctrines about instinct they saw fit to refute was that “contending for the identity of this faculty with reason in man,” which posited that “all the actions of animals, however complicated, are, like those of the human race, the result of observation, invention, and experience” (2: 469). Their special target was Erasmus Darwin’s Zoonomia, in which he argued that bees “learn” to adapt means to ends in cases where, when transported from a warm climate to a cold, they learn to lay up stores of honey for the winter. But, retorted Kirby and Spence, one only had to observe that bees were born knowing how to build hive cells and gather honey to refute Darwin’s unfounded assertion. Kirby and Spence believed that instincts were nearly unerring and required no learning. To them, the brain of the bee or spider was “impressed at […] birth […] with certain geometrical figures, according to which models its works are constructed,” whether webs or cells (2: 466). Instinct, they argued, “is not of a plastic nature”:

Without pretending to give a logical definition of [instinct], which […] is impossible, we may call the instincts of animals those unknown faculties implanted in their constitution by the Creator, by which, independent of instruction, observation, or experience, and without a knowledge of the end in view, they are impelled to the performance of certain actions tending to the well-being of the individual and the preservation of the species. (2: 471)

However, such a view of instinct did not prevent Kirby and Spence from denying insects a soul. Quite the reverse: to them, brain was synonymous with soul (“brain, alias the soul” [2: 466]), and both were analogous to the mind of God. But they based their analogy not on theological grounds, but empirical ones. Unlike either Paley or Erasmus Darwin, Kirby and Spence were extraordinary observers of insect behavior and observed a high degree of variation even among the instincts of members of the same species. This variation put to rest any notion that instincts proceeded with machine-like regularity. For example, they observed that while hive bees produce a regular hexagonal cell in nine instances out of ten, they occasionally produce an irregular cell. But far from an “imperfection,” they regarded these anomalies as adaptations of more or less regular behaviors to specific circumstances—evidence, in their view, of “calculated” behavior (2: 492). Attending to the wide variety of such calculations in many kinds of insect led them—if not toward claims about the intelligence of insects—away from any idea that instinct was merely mindless mechanism.

Rather than challenge the essential theological analogy, though, Kirby and Spence used their observations of the irregularities of instinct to advance a theory of divine perfection. For in fact, they argued, mechanical regularity of behavior would be a less wonderful demonstration of the perfection of instincts, an argument Charles Darwin would later employ in his argument for natural selection. In hive bees “there exists,” they wrote, “a moveable harmony in the mechanism by which cells are composed” (2: 492). Instinct may not be plastic, but the mind of God is. Thus they concurred with the eighteenth-century French entomologist Pierre Huber, who wrote that “it is not by a minute exactness that [Nature] marches to her end, but proceeds from irregularity to irregularity” (qtd. in Kirby and Spence 2: 494). “[A]pparent errors” reveal a “divine geometry” when we view them beyond the level of mere individual actions. Here, the mind of God makes regular and harmonious what might otherwise seem erroneous or anomalous. Huber, working hard to fit the “errors” committed by ants into a divine order, called these behaviors “preordained irregularities.” An enlightened divine analogy of insect behavior would therefore look beyond mechanical perfection to a more philosophical, divine perfection that accommodated variation, error, and irregularity. In this way, Huber, Kirby and Spence preserved entomology’s theological significance by modeling a more sophisticated divine psychology. In doing so, they opened the door to new ways of thinking about mind in nature.

Darwin and the Evolutionary Emergence of Intelligence

The instincts of invertebrates posed a major problem for Charles Darwin, one “sufficient to overthrow my whole theory,” he wrote (Origin 207). How could something as extraordinarily complex as the slave-making instinct in some ants, or the cell-building instincts of honeybees, have evolved from simpler forms? For that matter, how could human reason have evolved? Unless natural selection could explain such wonders it could not pretend to completeness. And if not complete, then not sufficient. The whole plan of the natural world depended on our shared mental history with the invertebrate world.[2]

Like his grandfather Erasmus, Charles Darwin knew that to preserve a distinction between instinct and intelligence was to preserve “the conventional distinction between animals and men” (Richards 108) that had buoyed the natural theologians, whose ideas about the fixity of species were the biggest obstacle to Darwin’s theory of species change. Even Darwin had to admit that nature came closest to the mind of God in the form of instinct. He wrote in his manuscript version of The Origin of Species that “it is most natural to believe that the transcendant [sic] perfection & complexity of many insects can be accounted for only by the direct interposition of the Creator” (Stauffer 466). He even regarded the cell-building instinct of bees to have solved a “recondite problem in geometry” better than the eye solved a problem in optics (466-67). Instincts, we might say, registered the perplexities of the order of nature “more perfectly” than did eyes.

It is perhaps calculated remarks like this that provide further confirmation for Clark’s sense that Darwin “may […] have referred to the example of insects to goad or to convert his opponents” (109). Indeed, experimental examinations of insects represented a direct affront to claims about the divine quality of insect instincts. They challenged basic theological assumptions about free will, human origins, and special creation in a contest between two competing analogies of mind: one divine, the other human. Were insects and other invertebrates windows onto the mind of God? Or did they illuminate the origins of mind in man? In the contest between these two analogies can be seen very clearly the theological obstacles to acceptance of his theory.

Despite his arguments with the natural theologians, Darwin regarded Kirby and Spence’s Introduction to Entomology as among the best work on the subject ever produced precisely because of their detailed observations revealed that perfection in nature implied something beyond mechanical regularity. But to Darwin, this perfection was not analogous to a higher order divine psychology—not, that is, to a more sophisticated God—but to the process of natural selection itself. The kinds of variations observed by Kirby and Spence allowed Darwin to develop a new analogy that would allow us to imagine how this otherwise unimaginable process could produce even the most refined instincts. There were, he recognized, no “fossilized instincts,” no behaviors or evidence of mind preserved in the geological record. Therefore “the sole guide is their state in other members of the same order and mere probability” (Darwin to Romanes, 16 April 1881; Romanes, Life and Letters 110). The only evidence for the evolution of instinct was to analogize from the present to the past: evidence of instincts in various stages of complexity in currently living species provided plausible analogies to stages of development in extinct forms. They offered imaginary evidence, or thought experiments, in how even the most complex behaviors might have evolved from less complex ones.

One of Darwin’s few published treatments of the matter of mind and instinct in the invertebrates is his chapter on instinct in The Origin of Species, where he discusses ants and bees. This chapter was an “abstract” of a longer chapter that was published posthumously, by his protégé George John Romanes, whose treatment of the subject I address below. In that chapter, both in abstract and in its longer form, Darwin confronted the question of the perfection of instincts, demonstrating in example after example—including many of those provided by Kirby and Spence—that instincts were neither perfect nor regular across a species: individual organisms frequently expressed instinctive behaviors in different ways. Furthermore, individuals frequently made mistakes.

For example, in the unpublished version of his chapter, Darwin discusses insects that feign death—a peculiar instinct, for which insects especially are “notorious,” due to the fact that death is “an unknown state to each living creature” and so cannot be the result of learning, memory, or experience (Darwin, “Appendix on Instinct” 363). Darwin was curious to account, therefore, for the “strange coincidence that the insects should thus have come to exactly simulate the state which they took when dead” (364). He examined seventeen different kinds of insects from “the most distinct genera” known to feign death, from “both poor and first-rate shammers,” and compared these with actually dead insects of the same species. What appeared to be perfect imitation of death turned out to be imperfect: “in no one instance was the attitude [of death] exactly the same” (364). Each insect, it seems, had its own interpretation of death.

Darwin showed a similar “series” or gradation of degree in “perfect” behaviors for the hive bees. He examined the “imperfect” comb of Melipona domestica (renamed Melipona beecheii), a hive-making stingless bee native to map iconMexico. These bees produce round honeycomb to store their honey, which Darwin saw as an intermediary example between the more architecturally advanced hexagons of Apis mellifera, or the European honeybee, and the more primitive, globular structures of bumblebees (Bombus), built only to incubate young. These intermediary and primitive stages showed by analogy that something as complex as the cell-making instinct of the honeybee could evolve from simpler nest-building instincts.

Furthermore, he found, bees frequently make mistakes in the construction of their wax cells: they often have to pull down their work and start again. Bees might inherit the behavior of economic comb-making, but that doesn’t mean that they do it perfectly every time. They are not simply machines outputting pre-programmed behaviors. Cell building is a process of trial and error and craftsmanship. Furthermore, “mistakes” in the craftsmanship of honeycomb could well turn out to be beneficial mutations that lead to improved overall design. Darwin hitched “imperfection” to a larger-order harmony in nature, but where Huber and Kirby and Spence posited an overall divine intelligence at play that harmonized the apparent disorder of animal behaviors, Darwin posited natural selection.

Analogizing from a present series of behaviors to a possible evolutionary genealogy, Darwin was able to show that instincts were subject to evolution in the same way that physiological structures were—that is, in incremental changes over long periods of time. Instincts may be wonderful, but they were no mystery: they were subject to natural selection just as “corporeal structures” were (Origin 209). Not only did Darwin’s study of instinct challenge the divine analogy, it opened the door to a human one: the behaviors of invertebrates could be compared to those of man. And if it could be demonstrated that we share mental affinities with insects and other invertebrates, then mind and brain were not distinct but unified at the level of behavior, and a comparative invertebrate psychology with a firm basis in evolution would indeed be possible.

As a starting point for such affinities, we can look back before The Origin to Darwin’s early notebooks on mind, when he was still working out his mechanism for species change. In his B Notebook on Transmutation of 1837-38, in which he first famously sketched his tree of life, he may have taken his cues of the question from his grandfather’s sensationalist philosophy. He had this to say about instinct: “People often talk of the wonderful event of intellectual man appearing,” but “the appearance of insects with other senses is more wonderful. Its mind more different probably & introduction of man nothing compared to the first thinking being, although hard to draw the line” (Darwin, B Notebook 222-23; B207-08, emphasis added).

A couple of things are interesting about this passage. First, it expresses Darwin’s interest in “the first thinking being”—that is, in the evolutionary emergence of mind. And second, it illustrates Darwin’s casual classification of “intellect” as one of the “senses,” suggesting, with Erasmus, a common basis for mind in the shared physiology of the senses. If intellect is a “sense” in higher mammals analogous to the senses of insects, then it was possible to imagine an origin of intelligence in lower order phenomena, like instincts. That is, intelligence might be an evolved behavior in the way that feigning death or cell-building are evolved behaviors. Darwin’s excitement about this proposition is palpable in his journal entry, perhaps because, as Richards points out, the thought “echoed Darwin’s then favorite philosophical author, David Hume, who characterized human reason as ‘a wonderful and unintelligible instinct of the soul’” (Richards 109; citing Hume, Treatise on Human Nature).

Given their radical physiological differences from us, invertebrates tended to raise these kinds of questions about the nature and the shared origins of mind. The comparison of intelligence to instinct had the power to shift the examination of the origins of mind to the register of behavior rather than physiology and anatomy. But despite his interest in instinct, these questions did not seriously influence Darwin’s canon of published works. Darwin tabled his interest in invertebrate minds for most of his career, confining his remarks to his “abstract” of his chapter on instinct in The Origin of Species. And in those short treatments, Darwin gave over his interest in the question of mind to a mostly economic view of natural selection—one which sought to explain the wonders of instinct through a Malthusian theory of population pressure and scarcity of resources, which reduces nature, “it must be admitted,” to “the grossest utilitarianism” (Darwin, “Appendix on Instinct” 383).

Mind All the Way Down

Most traces of Darwin’s earlier interest in behavior as a mechanism for species change had been eliminated.[3] But he never completely lost interest in the question of the limits of mind, and he revisited it in his final work, The Formation of the Vegetable Mould by the Action of Worms. Published in 1881 just six months before he died, this monograph expanded upon a paper he read to map iconthe Geological Society in 1837 just after he returned from his Beagle voyage, and so we could say that worms bookended Darwin’s career, though his concern for their minds featured only in the 1881 book. We could also say that Darwin’s Worms, as with many other of his scientific preoccupations, circled back to his grandfather’s natural philosophy. In the case of Worms, Darwin brought Erasmus Darwin’s philosophical study of instinct into the light of natural selection.

Worms is, of course, not Darwin’s best-known work of comparative psychology: this would be his 1872 The Expression of the Emotions in Man and Animals, in which he concentrated his attention on nearer mammalian cousins, showing our species-affinity with them at the level of emotional expression. Worms is more of a curiosity in Darwin’s career, though perhaps it better represents his lifelong interest in the “constantly repeated small and accumulative actions” of nature that produce large-scale change (Browne 490), and in it he lovingly and painstakingly described the process by which worms transform the world. In an acre of land, Darwin calculates, “a weight of ten tons of earth annually passes through [the] bodies [of worms] and is brought to the surface” (Formation 261), leading him “to conclude that all the vegetable mould over the whole country has passed many times through, and will again pass many times through, the intestinal canals of worms” (3-4) (see Figure 1).

map icon

A tower-like casting, engraved from a photograph

Figure 1: “A tower-like casting, probably ejected by a species of Perichæta, from the Botanic Garden, Calcutta: of natural size, engraved from a photograph.” Charles Darwin, _The Formation of the Vegetable Mould by the Action of Worms_ 124.

One curious effect of worm digestion is the sinking of objects on the surface, as worms dig beneath them and excrete the “vegetable mould,” or compost. Where objects appear to sink, they are in fact buried (see Figure 2).

Section through a fallen stone at Stonehenge, showing how much it had sunk into the ground

Figure 2: “Section through one of the fallen Druidical stones at Stonehenge, showing how much it had sunk into the ground.” Charles Darwin, _The Formation of the Vegetable Mould by the Action of Worms_ 156.

Darwin considered this act of burial a force of geology, but it began, curiously enough, with the mental habits of the worm. He was intrigued by the idea that such a force, hidden below the level of human perception, grinding the very surface of the earth into a “fine paste” (Formation 259) with its powerful gizzard, was possessed of something like mind. His experiments explored the limits of worms’ mental capacities, but also the limits of mind itself: how far down in the scale of nature can we look and still find evidence for psychology? But also, how far down, in a literal sense, does mind go? Worms can be found at depths of up to eight feet: they are responsible for the generation of soil and the character of landscape. In a real sense, the surface of the earth is a byproduct of the action of worms. The idea of locating mind there had the force of a secular critique of natural theology, for the lowly worm occupies the lowest level in depictions of the Christian Great Chain of Being.

In a reverse of Condillac, who endowed his statue with senses one by one as a thought experiment in the minimum criteria of mind, Darwin, in his assessment of the mental habits of worms, began with the familiar senses of mammals, and removed them one after another until he isolates their mental activity in a single sense. He first established that they cannot hear—“They took not the least notice […] of the deepest and loudest tones of a bassoon” blown near them (Formation 26). Further, they have no eyes, and so did not respond even when exposed to the light of a bull’s-eye lantern (20). They expressed some small sensitivity to temperature, but they possess but feeble sense of smell or taste. In general, Darwin’s worms demonstrated but one sense: touch. Touch alone is sufficient for the presence of mind, for by touch do they select and move material into their burrows, an activity that demonstrates their powers of intellect. Darwin set out to examine whether or not worms “learn” in any capacity through this single sense. Do worms produce sensory images (ideas) of leaves? Do they make judgments based on those images? For if, when given objects that were foreign to them, the worms dragged them all by the same manner as they dragged familiar objects, then they wouldn’t be exercising judgment, and instinct alone could be credited. But if instinct is excluded, then “intelligence alone is left” (67). Hanging on the judgment of a worm is, in fact, the whole of nature.

His measure in this experiment is man: “If a man had to plug up a small cylindrical hole, with such objects as leaves […] or twigs, he would drag or push them in by their pointed ends; but if these objects were very thin relatively to the size of the hole, he would probably insert some by their thicker or broader ends. The guide in his case would be intelligence” (Formation 66-67). Armed with this common sense analogy, Darwin set about giving his worms objects of varying size and shape and watched them work out how to go about inserting them into their burrows. He found that they “judged with a considerable degree of correctness” how to draw foreign material into their burrows (73), leading him to conclude that they “somehow gain a general notion of the shape or structure of pine-leaves, and perceive that it is necessary for them to seize the base” (78, emphasis added) as the best way to move objects. His worms had acquired a “notion, however rude, of the shape of an object and of their burrows,” suggesting even the capacity for ideation or abstract thought.

Based on comparisons with the ingenuity of man—or, rather, with the ingenuity of Darwin himself—Darwin felt his worms “deserve[d] to be called intelligent; for they […] act in nearly the same manner as would a man under similar circumstances” (Formation 99). But like Réaumur before him, he recognized that such a hypothesis will meet with natural antipathy: the philosophical and theological fortress that protects the human mind from the animal is not easily assailed. But, he says, we should remember we don’t know “enough about the nervous system of the lower animals to justify our natural distrust of such a conclusion” (100). The worm’s “[l]ow[ness] in the scale of organization” is no evidence of mindlessness. And anyway, brains are wondrous things: “we should remember what a mass of inherited knowledge, with some power of adapting means to an end, is crowded into the minute brain of the worker-ant” (100). The brain of the worm was a black box, known only by its outputs or behaviors, but its contents might be dimly glimpsed in the light of analogy.

George Romanes at the Limits of Mind

Darwin’s evidence of mind in the lower animals was based on a deceptively simple analogy: we can infer the evolution of complex mental faculties like intelligence by analogizing from the minds of invertebrates like worms to the mind of man. If we accept this analogy, then we can entertain the idea that even something as complex as intelligence can arise through natural selection. Looking at a worm fit leaves into its burrow is like operating a time machine, in which we can travel back to gaze upon ourselves at the dawn of reason. But if this sounds a bit like a recursive loop of analogy, that’s because it is: The analogy of the present to the past gave Darwin the means to suggest the emergence of the human mind at the end of an evolutionary genealogy that began with invertebrates, but it also meant assuming the existence of mind at the beginning of that genealogy, via the analogy with mental habits of the worm. To put this another way, Darwin didn’t so much create an evolutionary genealogy of mind: he assumed mind as the very condition of that genealogy. Darwin may have constrained the field of analogy, from a divine to a natural world source, but this shift was based as much on analogical thought experiment as it was on empirical evidence. Darwin’s common sense assumptions about the nature of mind at the lowest levels were anything but.

This is perhaps why Darwin never wanted to publish his notes on instinct. Showing common sense similarities in the behavior of worms and those of man was enough for him to provide what Michael Ghisellin calls “negative evidence” (42)—that is, the possibility of an evolutionary relationship could not be ruled out because we simply do not know what might be bundled into the neurons of the ant (or the worm). The invertebrate’s mind is a black box. In order to harness it as evidence of selection, Darwin had to shake it, but he didn’t necessarily have to open it. When the evolutionary biologist George John Romanes alluded to the curious fact of Darwin’s failure to publish his longer chapter on instinct in a letter, his mentor wrote back that the subject was “so much more interesting to observe than to write,” perhaps alluding to the elder man’s recognition of—and aversion to—the necessarily philosophical character of the subject (Darwin to Romanes, 19 June 1878; Romanes, Life and Letters 72).[4] Even in his own work on worms, Darwin never bothered to define the criterion of intelligence. These were, as Robert Young observes, “not his central concerns” (58).[5] To do more would mean venturing into theoretical territory and perhaps making a case for analogy as a genuine tool for scientific analysis that went beyond “mere probability,” speculation, and conjecture (Darwin to Romanes, 16 April 1881; Romanes, Life and Letters 110). Concerns about the value of speculation and conjecture had delayed the publication of the Origin as Darwin fretted over the reception of his “castle in the air” (Darwin to Lyell, 25 Nov. 1859; Darwin, Life and Letters 236). So instead, in his last work he relied on Romanes’s own remarks about intelligence in his Animal Intelligence (1882) (Darwin to Romanes, 16 April 1881; Romanes, Life and Letters 109).

Romanes, however, was willing to tread where Darwin wasn’t, and so he made a fitting successor to Darwin on the question of animal minds. The two engaged in lengthy correspondence on the subject until Darwin’s death in 1882, which Romanes took quite hard, having come to regard Darwin as a father-figure. Four years earlier, in 1878, Darwin sent Romanes his unpublished chapter on instinct along with permission to include it as an appendix in Romanes’s Mental Evolution in Animals (1883), the follow-up to Romanes’s Animal Intelligence. These two works together aimed to apply Darwinian selection to the question of intelligence and, more generally, mind. The first work he packed with examples of mental processes from the least complex animals to the most, while the second, which he regarded as likely to be the less popular, attempted to provide a grounding theory of mental evolution (Romanes to Darwin, 22 April 1881; Romanes, Life and Letters 117). With these works and Darwin’s unpublished chapter, Romanes set out to open the black box that Darwin had been satisfied to leave unopened. For Romanes, this meant developing Darwin’s analogy between human and nonhuman minds beyond common sense, into a tool that could provide the scientific basis for a comparative psychology by looking at the lowest limits of evidence for mind.[6]

Romanes based his theoretical work on experiments with the nervous system of the Medusae or jellyfish. His research represented the experimental limits of physiological inquiry into the brain, in the nervous tissue of invertebrates. At the time, the existence of a central nervous system in the Medusae was controversial. In 1869, T. H. Huxley asserted in Classification of Animals that “no nervous system had yet been discovered in the Medusae” (qtd. in Romanes, Life and Letters 16). While some had observed nerve-like apparatus in some forms of Medusae in the “fine fibres running along the margin of the swimming bell,” no one had yet determined that they did indeed operate as nerves. Romanes, however, in Jelly-Fish, Star Fish, and Sea Urchins: Being a Research on Primitive Nervous Systems (1885) succeeded in demonstrating that reactions in the nerve tissue in the Medusae bore “striking resemblance” to reactions in “higher” order animals and concluded that the nervous system made its first appearance on the evolutionary scene in the Medusae (Romanes, Life and Letters 16).

His physiological experiments led him to investigate the lower limits of mind itself, and by the mid 1870s, Romanes was devoting himself more and more to “philosophical natural history” (Life and Letters 13). Romanes sought to locate connections between physiological and mental phenomena, a pursuit that was at the core of his “Monist” philosophy, which challenged the Cartesian “dualism” that was responsible for the separation of mind and brain. Monism built upon the philosophical assumptions of the earlier Romantic sensationalists like Erasmus Darwin, for whom there was continuity between the input of the senses and mental capacities like memory, learning, reason, and choice. Contemporary proponents of Monism included the German evolutionary biologist Ernst Haeckel and, as I’ll discuss further on, the Swiss myrmecologist and psychiatrist August Forel.

Monism assumed a basic hierarchy of mental states, starting at the bottom with reflex action, which Romanes defined as an “inherited mechanism of the nervous system formed to respond to particular and often recurring stimuli” (Animal Intelligence 17). Reflexes might adapt to circumstances, but they do not reveal intention or consciousness. Next was instinct, defined as “reflex action into which there is imported the element of consciousness,” if not full-blown consciousness itself (Animal Intelligence 17; Mental Evolution 159). Though instinct comprises “faculties of mind which are concerned in conscious and adaptive action,” it does not involve individual conscious experience. Instincts are notable for their regularity across a species. For example, all chicks peck at the ground straight out of the shell. Instinct is also notable for the separation of means (pecking) from ends (food). A chick will peck regardless of whether or not it obtains food from its pecking.[7] At the top was reason or intelligence, or the ability to adapt means to ends. With reason, an organism can employ what it learns in one circumstance to a “novel” context (Animal Intelligence 17). It therefore implies conscious experience. According to Romanes, reflex action, instinct, and intelligence were not different in kind: they graded imperceptibly into one another all the way down the chain of complexity, even to animalculae or microscopic organisms, where “[a]ny distinction between the mental and non-mental should be obscure, and generally impossible to determine” (Animal Intelligence 13).

Romanes’s philosophical natural history led him to inquire even into the nature of nervous impulses prior to the existence or development of the physiological “channels” (i.e., the “fine fibres”) through which nervous impulses pass. “Reflex action,” he speculated in a letter to Darwin, “ought to be present before the lines in which it flows are sufficiently differentiated to become distinguishable as nerves” (Romanes to Darwin, 20 July 1875; Romanes, Life and Letters 33). Speculations like this and his correspondence with Darwin around the time the elder scientist was writing Insectivorous Plants (1875) reveal that Romanes was speculating about mind beyond (or perhaps below) the lowest forms of animal life, seeking analogies to nervous system development even in plant physiology.

The Limits of Objectivity

Ethel Romanes’s characterization of her husband’s later work into mind as “philosophical natural history” is apt because, despite Romanes’s award-winning experiments into the nervous systems of invertebrates, the core of his work on animal intelligence and mental evolution took him well beyond the reach of objective science—a fact some regarded as “unfortunate” (Life and Letters 13). We cannot, Romanes thought, observe the mental activity in other organisms directly (16). We can only observe mind indirectly, through behavior. Behaviors were like “ambassadors” of the mind, communicating between the mental activities of an organism and the mind of the observer. From these ambassadors, we have to infer the presence or absence of mind. Neither can we use the subjective—i.e., first-person—experience of another organism to determine the presence or absence of mind. Organisms like jellyfish cannot report the quality of their subjective experience because they lack language to do so. Therefore, we cannot know definitively what it is like to be another organism.

Relying on casual inferences based on observable behaviors was, of course, Darwin’s common-sense approach to the analysis of mental states in animals, like worms. Darwin did not bother to defend this approach, which relied on the mind of the investigator as the comparative standard for mental phenomena. For him, if something looked like rational choice or learning, then this was good enough to infer that it is. But this common-sense approach implicitly placed mind beyond the reach of science, in a black box. We cannot know for certain what the brain of an ant or worm is capable of. So in his argument for the possibility that natural selection could produce something like instinct or intelligence, Darwin relegated mind to the category of “negative evidence”—that is, unprovable, but therefore no argument against its possibility.

Romanes was not equally satisfied to leave the question of mind undisturbed, though he did recognize the special challenges that mind presented: it presented the limit of both objective and subjective analysis. As a way forward, Romanes started with the only thing we can be absolutely sure of: our own consciousness—that is, our subjective, first-person experience of the world. Romanes argued that when studying other minds, we “project” the “known patterns” of our own minds onto the “blank screen” of other organisms to produce an “eject.” We use this projection or eject to infer the existence or absence of mental activity (Mental Evolution 16).[8] That we can do this comes from some circular reasoning: conscious experience allows us to determine mental activity in other organisms; but conscious experience is something “we have without having to establish that we have it.” In short, it is the “ultimate” and therefore indefinable criterion of mind. Having conscious experience makes us experts in mind simply by virtue of having conscious experience. Conscious experience is therefore the best—but admittedly, he adds, the only—tool for determining mind.

Ethel Romanes called her husband’s work “philosophical” because she recognized that many would have regarded it as unscientific, an opinion she herself may have held: she suggested that had he lived, her husband would have eventually become more “experimental”, meaning more scientific (Life and Letters 13). But this seems to get it wrong. George Romanes seemed to recognize that experimental work, in the sense of physiological experiment, could not produce objective certainty of mind; with mind, he had reached the limit of objective, experimental science. And so he had to invent a new science, and a new kind of experiment—the eject—in order to establish the existence of minds outside our own. For Romanes, the eject was an analogical thought experiment on par with objective science. With the eject, Romanes attempted to give Darwin’s common-sense analogies of (human) mind philosophical grounding and, therefore, scientific validity.

Challenging the Criteria of Mind

The eject is in essence a science of compelling analogies. Romanes chose not to approach the question of mind through traditional checklists of criteria such as consciousness, choice, learning, memory, and ideation. Such criteria, he noted, were the tools of skeptics: in their application, more often than not, they prejudice us against the existence of mind. Romanes instead challenged those criteria by locating analogies for them in their “obverse,” that is, in nerve processes and organisms we least associate with mental faculties. He aimed to show that we cannot know whether we are in fact observing a higher or a lower order phenomenon, ultimately aiming to collapse the distinction between higher and lower and thereby open up possibilities for mind in even the least likely places.

For example, he demonstrated that the complex cerebral hemispheres, which we associate with the highest level of mental process, consciousness, “closely resemble” those lesser structures, the ganglia or nerve centers which we associate with the lowest processes, reflex action. The operations of the cerebral hemispheres constitute an “obverse reflection of ganglionic action” (Mental Evolution 35). This is to say, there are compelling physiological analogies between both the highest level of mental functioning and the lowest. These structural analogies permitted him effectively to erase the differences: “There can,” he says, “be no reasonable doubt that the mode of their operation is substantially the same” (35).

Given this parallel structure, Romanes needed different criteria, preferring common sense analogies that amounted to a “we will know it when we see it” approach. For example, rational choice: If “the distinctive element of mind is consciousness, the test of consciousness is the presence of choice,” and the evidence of choice is uncertainty (18). But here again, Romanes declined to explain the criteria, or explained it rather circularly. We use, he says, choice to describe those actions performed “by agents who in virtue of the non-mechanical nature of these actions prove themselves to be mental, or by agents already recognized as mental i.e., by agents who have already proved themselves to be mental by performing other actions” of a “nonmechanical or unforeseeable nature” (Mental Evolution 19, emphasis added). In short, just as consciousness is something we have without having to establish that we have it, the actions of any “nonmechanical” agent are, “we feel assured,” attributable to choice simply by virtue of their nonmechanical nature. We wouldn’t, for example, ever mistake a complex machine for a conscious one, despite that it may be impossible to predict the result of its actions, because we a priori identify complex machines as non-mental. The impossibility of predicting its choices doesn’t affect our ability to doubt its mind because we operate, he thought, with a common-sense understanding of mind. A machine is not an organism, and second, would stretch the analogy too far to attribute mind to it.

But whereas a machine might provide the absolute limit of mind by virtue of its mechanical nature, the same cannot be said of a sea anemone. Even an anemone “chooses” among stimuli, such as when it fails to react when struck forcibly with jets of water, but does react when its arms come into contact with a solid body (Romanes, Mental Evolution 51-52). The anemone’s “choice” to grab at the stimulus of a physical body but not at the motion of water is just the most primitive expression of reason. Romanes further argued that even something that seems definitively without mind, such as the nervous apparatus of the stomach, might be said to learn to adapt its behavior according to the “requirements of its individual experience” to a degree “that were the organ an organism we might be in danger of regarding it as dimly intelligent” (21). In this way even the behaviors of things “not concerned in the phenomena of consciousness,” such as stomachs, might nevertheless deductively suggest the presence of mind.

Ideating Sea Polyps

What then, beyond inorganic objects does not express mind? The force of analogy is such that, once one has made a plausible or “common-sense” analogy between humans and non-humans, there doesn’t seem to be any stopping. For example, Romanes argued that “ideation”—another higher-order mental functioning—may be analogous to coordinated muscle movement because the two kinds of coordination share evolutionary parallels. Coordinated muscle movements evolved from disorganized ones to produce organized actions, such as when “in eating, the act of opening the mouth mechanically follows the raising of the morsel,” a sort of action that “is as true of the polyp as of the man,” and which “manifests itself long before the dawn of any of the powers of the will” (Mental Evolution 43).

Ideation, likewise, is the gradual coordination of various mental activities into the ability to produce abstract thought, which is, in turn, the ability to make organized associations among ideas, such as when we combine existing memories to imagine an experience we have not yet had. The analogy, he thinks, is grounded in evolutionary physiology: eating is a mechanical act of the association of muscle movements; this association of muscle movements is analogous to the association of ideas; both kinds of associations share a “common source in the nervous system” (Mental Evolution 39); therefore, the muscular movements of a polyp can be regarded as an evolutionary analogy for subjective ideation.

One has only to imagine a sea polyp (id)eating on the ocean floor to recognize the compelling absurdity of Romanes’s thought experiment. And that, I would argue, is its aim: to render the analogy plausible merely by thinking it. Given that no “more precise parallel between these two manifestations of nervous machinery,” eating and ideating, is imaginable, it requires no further scientific analysis, for “it has been perceived by the common sense of mankind” (Mental Evolution 44). Common sense teaches us the nature of mind, even if we can’t always hear its lessons. If we find ourselves skeptical of the analogy, we need only examine our idioms, as when we apply the term “gymnastics” in a sense both physical and mental (44). In such phrases we express the truth of the analogy even, perhaps, before we fully grasp it. Our minds, free of prejudice against other minds, are the best tools of our scientific understanding of mind.

Against Skepticism

The comparative psychologist C. Lloyd Morgan suspected that Romanes might have been gaming his science through such wordplay. In a response to Romanes, Morgan accused him of smuggling mind into his very definitions. For example, in Mental Evolution Romanes implied that instinct was a “lapse of consciousness” (Morgan, “Instinct” 372)[9]: at some point in the evolutionary past, he claimed, an organism’s conscious choices became so habitual that they eventually became inherited behaviors. In this way, Romanes posited consciousness some time in the evolutionary past for behaviors we would now regard purely as non-mental, mechanical instincts. But as Morgan argues, if you can import consciousness this way into an organism’s evolutionary history simply through your definition, there is no reason not to do the same for intelligence. Therefore, “instinct and reason run together” (“Instinct” 373) and science devolves into mere “word philosophy” (Romanes to Darwin, 6 Feb. 1880; Romanes, Life and Letters 95).

This argument illuminates an important difference in the approach to comparative psychology, particularly as the two men shared almost identical premises. Like Romanes, Morgan believed in the union of mind and brain. And like Romanes, Morgan believed that the mind could be studied only through inference and analogy. But these premises led Morgan to an opposite conclusion. To him, the mind was a black box: we can infer little of consciousness from the actions of other beings (“Instinct” 374), and thus he maintained the essential otherness of other minds.

Romanes would have counted Morgan among the skeptics, whom no argument would satisfy because they continued to doubt that “mental processes […] accompany objective activities,” except of course in the case of the doubter’s own objective activities (Mental Evolution 23). To Romanes, this sort of skepticism of mind was his era’s equivalent of Réaumur’s critics, prejudiced against the soul of the insect. Romanes called out what he regarded as the unreasonableness of this prejudice, noting that any skepticism strong enough to deny that mind-like behavior proves the existence of mind must also be strong enough to deny even the existence of mind in “higher” order animals, including in the skeptic himself (Animal Intelligence 4)! However, we can save ourselves from this sort of infinite skeptical regress with common sense, which, he argues, can overcome the need for “impossible evidence”: through common sense, we “feel” the connection of animal and human mind, despite obvious differences in physiology or evolutionary history.

But Romanes’s common-sense analogies did not stop at parallels between the nervous system and the “higher” mental faculties. Think of a spider that uses a stone to balance its web. Now think of a spinning jenny, a machine whose coordinated movements “rival those of the tight-rope dancer.” Similar to a spider with a stone, with the spinning jenny “the necessary connexion between the advance of mental discrimination and muscular coordination was severed” (Mental Evolution 59). Just as at the lower levels we can make no distinction between mind and not-mind (remember the polyp), the machine makes possible muscular development not limited to actual muscles. With the jenny, human mental development reaches out into space to express a psychology no longer bound to actual brains. Presumably, one could study human psychology by studying the operations of the spinning jenny in a form of industrial psychology.

Elsewhere, as we’ve seen, Romanes restricted consciousness to the domain of organic beings, which located a fundamental limit to mind in the special “nervous tissue” which is “so sparingly distributed through the animal kingdom” (Mental Evolution 24). But with the inclusion of industrial machinery, Romanes removed that limit. What began as Monism—mind in the brain—has now, through analogy, evolved mind beyond the brain, leaving open the possibility that everything is a potential source of mind. In stark contrast to Morgan’s skepticism, Romanes demonstrated his willingness to grant mind-likeness not just to polyps or even stomachs, but to inorganic machinery. Mind, he believed, spills over into the world, overflowing even the common sense limits of shared physiology. In analogies like the spinning jenny, Romanes demonstrated that his invertebrate psychology had become an investigation into our own mind’s ability to recognize and accept the compelling analogies to mind-like behavior in nonhuman animals. But rather than obscuring the possibility of mind, this approach in fact opened up the possibility of a mindful universe, advancing a radical non-skepticism akin to faith.[10]

Spiritualist Analogies

One final analogy will perhaps highlight the metaphysical nature of Romanes’s faith in a comparative psychology. Romanes, unsurprisingly, was interested in spiritualism. In this regard, he was, like his contemporary Alfred Russell Wallace, a man of his times. According to Ethel Romanes, George “never could assure himself that there was absolutely nothing in spiritualism, no unknown phenomena underlying the mass of fraud, and trickery, and vulgarity which have surrounded the so-called manifestations” (Romanes, Life and Letters 48-49). Ethel Romanes framed her husband’s interest in spiritualism as an expression of his religious sensibilities, which, though suspended for doctrinal reasons, he never fully abandoned.[11] “His was a religious nature,” she asserts, but having become intellectually active in the years after the publication of Darwin’s Origin of Species he understandably underwent a painful “period of conflict between faith and scepticism.” Despite his work in experimental physiology, he could never accept, as Darwin did, “a purely materialistic position” (79). In her view, her husband’s scientific study was not a displacement but an expression of his religious nature: she observed a parallel between his philosophical natural history and “the deepest and ultimate problems of theology” (84). If we accept this characterization, then one might convincingly argue that Romanes sought to synthesize science and theology by way of comparative psychology, and that his science amounted, in essence, to an extended theological analogy: that a belief in the existence of mind in the lower nonhuman animals would itself be analogous to a religious faith that the “law, order, and beauty in the universe” are manifestations of a divine mind (81). Romanes may have returned to a natural theology, this time from within the constraints of natural selection.

Jean-Henri Fabre’s Psychology without Evolution

Romanes’s theological analogy points, perhaps, to a late-nineteenth-century unease with the economic materialism that ultimately lay at the foundation of Darwin’s theory of natural selection. In this regard, Romanes finds an unlikely bedfellow in an entomologist who arrived at invertebrate psychology from a non-evolutionary perspective. French entomologist Jean-Henri Fabre demonstrated that analogies between the minds of human and nonhuman animals do not depend exclusively on the theory of natural selection.

Though they were close contemporaries, Charles Darwin and Jean-Henri Fabre are a study in contrasts. Where Darwin came from a family of scientists, Fabre was born to a poor, uneducated family of farmers and unsuccessful shopkeepers. Where Darwin, grandson of a famous natural philosopher, could claim to have been “born a naturalist” (Barlow 23), Fabre reports this reaction from his mother, after returning home as a child with stones and bugs: “Green stuff I don’t mind, it does for the rabbits. But stones that tear your pocket out, and poisonous animals, what good are they, silly? There’s no doubt about it, someone’s cast a spell on you!” (Fabre, Life of the Fly 174). Darwin’s family was wealthy and well connected, which facilitated his presence on board the Beagle and thus his future as a gentleman-naturalist. Fabre’s poverty, on the other hand, forced him to abandon his love of natural history to support himself through secondary-school teaching, which in map iconFrance at the time made no allowance for natural science. He even went as far as to lock away his books on natural history so as not to be tempted by them while he devoted himself to more sustaining pursuits. Darwin could pursue his science with unbroken attention, settling down permanently after his marriage like a barnacle at map iconDown House in map iconSurrey, from which he corresponded with fellow naturalists in a vast global network. Fabre only returned to his beloved insects late in life, finally scraping enough to buy a small property in the southern French countryside, the Harmas, where he confined his attention to the insects that shared his immediate environment.

But their most important contrast, from a scientific point of view, was over evolution. Darwin of course was an evolutionist, having refined the mechanism of species change, and whatever else his research entailed, all his inquiry into the behaviors of plants and animals was done in support of his theory of natural selection. Fabre was an anti-evolutionist. As a religious man, “he maintained throughout his life a stubborn belief in divine creation and the fixity of species” (Grant 397). He pursued his insect research with purposes other than establishing continuities between man and the invertebrates.

But Fabre’s religiosity did not prevent him from becoming an astute and important experimental investigator. In fact, Darwin was a great admirer of Fabre’s Souvenirs Entomologiques (1879): “Never,” Darwin wrote to Fabre, “have the wonderful habits of insects been more vividly described, and it is almost as good to read about them as to see them” (Darwin to Fabre, 31 Jan. 1880; Darwin, Life and Letters 220). He delivered this praise even though Fabre insisted not only “so strongly on the unvarying character of instinct,” which Darwin (and Kirby and Spence) had refuted, but against natural selection (Darwin to Romanes, 16 April 1881; Life and Letters 111). The two men corresponded briefly on such topics as the sense direction in insects, as well as on Fabre’s own resistance to Darwin’s theory. “I am sorry,” Darwin wrote to Fabre in 1880, “that you are so strongly opposed to the Descent theory; I have found the searching for the history of each structure or instinct an excellent aid to observation […]. If I were to write on the evolution of instincts, I could make good use of some of the facts which you give” (Darwin to Fabre, 31 Jan. 1880; Darwin, Life and Letters 220). In a conversation about observations in his grandather’s Zoonomia of a wasp cutting off the wings of a fly, Darwin agreed with Fabre that the practice illustrated was “generally” instinctive, but, he added in good nature, it must be attended by “une petite dose de raison.”

Perhaps because Fabre did not subscribe to Darwin’s theory, his rather anomalous explorations of insect instinct provide a rare and fascinating picture of the kinds of ideas about psychology and mind that can emerge outside an evolutionary framework. Fabre took his cues from Réaumur, who put animal behavior above anatomy and morphology in drawing relationships among animals. Fabre writes, “propensities and aptitudes do not depend exclusively upon anatomy; high above the physical laws that govern matter rise other laws that govern instincts” (Wonders 42). More important than anatomical science, more important than “the number of joints in a Crustacean’s antenna” (15), is a “universal psychology.” He called his insects the “documents” of this psychology, much as Romanes considered animal behavior an “ambassador” of mind, but he set out to challenge the correspondences between man and invertebrate that Darwin and Romanes sought to reinforce. He aimed “to establish by experiment the line of demarcation between intellect and instinct; to prove […] whether human reason be an irreducible faculty or not” (15). The Harmas was to be his laboratory for the investigation of “the instinct, the habits, the manner of living, the work, the struggles, the propagation of that little world” of insects that lies so near to us yet so far from our perception. The marvelous world of insects provided insight into the nature of reason: they challenged a Monistic philosophy, asking, is the stuff of mind reducible to the physiology of brain?

Fabre’s Cabinet of Insects

In each of his detailed experiments, Fabre found the answer to be emphatically no. In one, he queried claims made about the “psychical capacities” of a “celebrated” insect: beetles of the genus Nicrophorus, which possess the unusual instinct of laying their eggs on small dead animals like birds and mice they find laying about. But first they have to bury it, hence their nickname, the burying beetle, and the colorful epithets applied to their many species: Nicrophorus sepulchralis; Nicrophorus funeraris; Nicrophorus humator.

“This undertaker,” writes Fabre, “is endowed, they say, with intellectual faculties approaching reason” (Wonders 62). Like Darwin’s, Fabre’s manner of testing such claims involves the examination of the animal’s “fixed methods” (67). That is, for the beetle to employ reason, it must, when “[e]xposed to fortuitous hazards,” “be able to modify his tactics within the limits of his modest perceptions” (67). Does the beetle’s peculiar, funereal instinct suggest “the gleams of reason? Have you within you,” he asks in his characteristically conversational style, “the humble germ of human thought?” (63). Or is this assumption just another of the “philosophical brutalities” we perpetrate upon insects?

First, Fabre demonstrated how they bury. He placed a small dead mole on loose, sandy soil and waited. “The body,” he reports, “seems to disappear of itself,” as the sand that has been excavated from beneath it “slips into the pit and covers the interred Mole […]. For a long time yet, until the depth is regarded as sufficient, the body will continue to descend” (69) into the earth. “It is,” he says, “a clandestine burial.” Then he proceeded to test the resourcefulness of his beetles using ingenious and darkly comical means. Indeed there’s a gallows humor to his experiments. He places a carcass on unyielding ground. They can’t dig: will they move it? Eventually they do.

A mole

Figure 3: “The mole is fixed fore and aft, with a lashing of raphia, to a light horizontal cross-bar resting on two forks. The Necrophor, after long tiring themselves in digging under the body, end by severing the bonds.” Jean-Henri Fabre, _The Wonders of Instinct_ 84-5.

But what if he suspends the carcass above the ground, on a couple of sticks: how will they get it down? (see Figure 3) Another he suspends in a branch: will they know enough to undermine it? (see Figure 4) Yet another carcass he strings up in a kind of gibbet and watches whether they register that the body doesn’t descend when they excavate beneath it (see Figure 5).

A mole suspended on a stake

Figure 5: “The stake is slanting; the mole touches the ground, but at a point two inches from the base of the gibbet. The Burying-beetles begin by digging to no purpose under the body. They make no attempt to overturn the stake. In this experiment they obtain the Mole at last by employing the usual method, that is by gnawing the bond.” Jean-Henri Fabre, _The Wonders of Instinct_ 92-3.

A mouse in the branches of a tuft of thyme

Figure 4: “A dead mouse is placed on the branches of a tuft of thyme. By dint of jerking, shaking and tugging at the body, the Burying-beetles succeed in extricating it from the twigs and bringing it down.” Jean-Henri Fabre, _The Wonders of Instinct_ 88-9.

Occasionally the beetles succeeded in solving tricky problems, but on balance no more often than can be attributed to chance. In fact what appears to be problem solving is more often simply accident. “[W]e shall seek in vain for any indication of reflection,” he says. The beetle, “in spite of his legendary renown, […] has no guide but the inconspicuous promptings of instinct” (100).

A further experiment involves the pine caterpillar, an animal “sheeplike, not from foolishness, but from necessity […]. They proceed in a single file, in a continuous row, each touching with its head the head of the one in front of it” (119). The lead animal puts down a silken thread for the others to follow, and this is their only guide: he established that they possess no vision, no hearing, nothing but this thread. The thread of the pine caterpillar is the minimum of its mental capacity. Fabre is interested in testing the limits of this behavior: how far will this following instinct go? To what ends will the caterpillar follow the leader? “What tricks can I play upon them?”, he asks.

First he removed the lead caterpillar, but the procession rolls on with a newly promoted leader. Then he broke the silken cord, but this too fails to stop the train. When he removed an animal from the middle of the procession and cut the silken cord, the procession simply split in two, but otherwise continued without disruption. But then he tried to get the caterpillars to “describe a closed circuit” (127)—a nasty trick indeed. “Will they persist in following a road that never comes to an end?” This proved challenging for the experimenter, and we are privy to the mind of the scientist as he tried increasingly ingenious methods by which to effect unnatural experimental states. A closed circuit of caterpillars is the artful invention of behavioral psychology.

After some trial, he succeeded in getting his caterpillars to walk a circuit around the edge of a large vase. In such a procession “there is no longer a leader.” “I said to myself: ‘The procession will go on turning for some time, for an hour, two hours, perhaps; then the caterpillars will perceive their mistake. They will abandon the deceptive road” (130). “Facts, however, forced me to accept the incredible” (131). “My success goes far beyond my wildest suspicions… I am stupefied.” He began the experiment in the afternoon. The caterpillars trudged on despite the lapse of nine hours, well into evening and “grazing time” for the insects. While other caterpillars at their liberty descended from their greenhouse haunt “to browse upon the pine-branches,” these “poor wretches, foolish slaves of their ribbon […] cannot make up their minds to do so” (132). “I leave the famished ones at half-past ten” and returned at dawn. At first they were motionless, but as they warmed, they continued their endless circuit with “machine-like obstinacy” (133).

The final tally? Eight days of walking through cold and heat and hunger and disorder: he calculated that within those eight days, allowing time for stopping, the animals walked for eighty-four hours, a total of 453 meters or more than a quarter mile. His conclusion: “The school most highly honored today”—that is, the school of evolutionary theory—“is very anxious to find the origin of reason in the dregs of the animal kingdom. Let me call attention to the Pine Procession” (141).

In such demonstrations of animal stupidity, Fabre hoisted his insects on the petard of instinct. But in other experiments his insects took on more analogical proportions. In one extended analogy, Fabre’s investigation of the physiology of the Black-bellied Tarantula, the Narbonne lycosa, led him to liken it “in no small measure to our industrial machines.” The spider’s expenditure of energy, through constant exercise of its fibers, “demands […] the renovation of its organism.” “Warmed by its food, the animal machine moves, walks, runs, jumps, swims, flies, sets its locomotory apparatus going in a thousand manners” (166). And in this, he thinks, “we can compare it with the locomotive engine.” “As the iron horse performs its work, it [too] gradually wears out its pistons, its rods, its wheels, its boiler-tubes” (165). And what does the engine eat but “plastic food” in the form of coal, and what is the engine’s coal consumption but “browsing the ancient foliage of arborescent ferns in which solar energy has been accumulated” (167) over eons? “Life,” he concluded, “is a fire-box.”

In this analogy, the engine becomes more animal in proportion as the spider becomes more mechanical. The Lycosa would seem a Cartesian “beast-machine,” a clockwork animal without reason or will. But Fabre’s machine analogy differs from Descartes’s in important ways. “An idea suggests itself,” he writes. “We say to ourselves that, without being life, a machine is something more than matter, for man has added a little of his mind to it.” Fabre here proposes something like artificial life in the machine; for him, a machine animated by the mind of man is analogous to an insect animated by the mind of God.

Fabre’s machine analogy shifts the frame of reference beyond the human, to a non-anthropomorphic psychology. But he takes this even further, in the case of the Banded Epeira, a spider capable of producing webs up to 2 meters in diameter (see Figure 6).

The Banded Epeira

Figure 6: “The Banded Epeira inscribing her flourish after finishing her web,” and “The Banded Epeira letting herself drop by the end over her thread.” Jean-Henri Fabre, _The Wonders of Instinct_ 172-3.

Using another technological analogy, the web of the Epeira can, Fabre thinks, be likened to a telegraph wire; “It is like a telephone capable […] of transmitting infinitesimal waves of sound,” of information, over long distances. “The spider,” he says, “listens with her leg” (201). This “animal machine” produces a system of communication analogous to the human telegraph. The web embodies the intelligence of the spider and is thus an extension of the animal’s mind. That is, instinct and intelligence result in the same product—a communications network. These animals don’t think like us: they are radically different. But their mindless instincts affect products analogous to those of human intelligence.

Fabre here employs an analogy strikingly close, if not identical, to Romanes’s. Romanes, as I discussed above, analogized a spider employing a stone in its web for balance to the human invention of the spinning-jenny, in which mind in both its simplest and most complex forms graduates beyond the brain to include its environment. But for Fabre, the analogy depends on keeping insects and intelligence distinct.

Unlike Descartes, Fabre’s machine analogies allow him to shift to another model of intelligence, one that includes both animal and machine. If animals and machines share behaviors, then they share an essential psychological affinity. A “stupid” arthropod might well be a “smart” machine. We wouldn’t call a machine that can do what a spider can do “stupid.” We might in fact be elated to build a machine with behaviors so complex. Therefore, we should evaluate them along a different axis than the intelligence/instinct axis. On that axis, the invertebrates lose every time. The force of Fabre’s comparative psychology is to help us to understand the mind of organisms that are radically other. He calls them stupid, but this is not to devalue them. He needs to make them “stupid” before we can see their minds.

Mind in Nature

The important thing to note here is that the behaviors of insects produce effects that are comparable to human intellect, but which are not intellectual. This is why, when viewed from the outside, such automatic behaviors often appear intelligent. But that’s a mistake. And only by close scrutiny and experiment does Fabre reveal the true nature of their minds. Fabre used the same methods of Darwin, the same analogies of Romanes, but his premises were different: he didn’t believe in evolution, and thus in an unbroken chain from the invertebrate to the mind of man. And so he arrived at a radically different model of mind.

But it is precisely this lack of belief in evolution that allows him to dream up a model of mind that takes mind beyond the brain, but without either being a Cartesian dualist or a Monist. He imagines mind as an emergent phenomenon—something that arises out of, or emerges from, simpler processes, but which is not reducible to those processes. It takes something from outside our minds to recognize the phenomena beneath the pattern, or that there is a pattern at all. Fabre—unrestrained by the evolutionary model—attempted to get at the question of intelligence and even consciousness from outside the brain, using what is most alien to us: the psychology of invertebrates.

August Forel’s Myrmecological Theory of Mind

Romanes argued that the “eject” was necessary because there is no way to study the mind of invertebrates from “the inside”—that is, from their own subjective experience of the world. But what might a psychology of invertebrates look like from the inside? What is the experience of the invertebrate mind? This question drove the Swiss myrmecologist August Forel (1848-1931) to fuse his lifelong interest in ants with his psychiatric pursuits.

Forel began his study of ants as a child of eight. A shy, isolated, and physically stunted boy, Forel’s ants provided him solace as well as an education. Like his predecessor, the nineteenth-century naturalist Pierre Huber, Forel “vowed to myself that I would become […] an historian of the ants,” (Out of My Life 79). As a boy of eleven he made careful study of them, discovering lestobiosis, or the thieving practices of some ants, which had escaped even Huber, and which would become the subject of his first scientific publication. He went on to make observations that Fabre would later confirm, and even correct mistakes made by his hero Hubert as well as by the much earlier Réaumur. He published his 3-volume Ants of Switzerland in 1874, for which he was awarded the Swiss Natural History Society’s Schläfli prize, and his 5-volume opus The Social World of the Ants Compared With That of Man in 1923 (see Figure 7).

Three ants

Figure 7: August Forel, _Le Monde Social des Fourmis (The Social World of Ants)_, Vol. 3, Plate 2.

Forel’s interest in the anatomy and physiology of ants also fed his interest in psychiatry and brain-science. As a young doctor, he helped to perfect the microtome, the instrument for slicing very thin sections of organic matter, and succeeded—he boasted—in “making the first microscopic section of the human brain” (Out of My Life 93). Brain anatomy was crucial to Forel’s exploration of mind, for it was, he wrote in his memoir, in a physiology-based study of mind that he was to find “the contact of brain and soul” (63)—a sentiment that expressed the intersection of his Monist philosophy and his incipient psychology.

Like his fellow Monist Romanes, Forel’s psychology was premised on dissolving the distinction between instinct and intelligence through the mechanism of natural selection. He described instinctive behaviors as “not inherited habit, but phylogenetically inherited intelligence which has gradually become adapted and crystallised by natural selection or by some other means,” he wrote in a short but important methodological treatise of 1904, Ants and Some Other Insects: An Inquiry into the Psychic Powers of These Animals (12) (see Figure 8).

Cross-sections of ant brains

Figure 8: Magnifications of the brains of worker, queen, and male ants, seen from above. August Forel, _Ants and Some Other Insects_ 15-6.

The manner of this dissolution seems to echo both Darwin and Romanes, who agreed that actions at first directed by reason could, by “frequent repetition,” become so habitual as to become instinctive. Darwin’s example of this was the Pompilius wasp that stings caterpillars or spiders in such a way as to paralyze but not kill. Its larva, hatched from eggs laid on the paralyzed prey, may then feed on fresh rather than dead food. How the wasp came to “know” to perform this action, Darwin surmised, arose through trial and error, which implied conscious choice and learning: It did not to him seem unreasonable to suppose that they “observed by their intelligence” where to sting, nor did he find it “at all incredible that this action should thus become instinctive” through natural selection. Darwin regarded such instincts as a form of species “memory transmitted from one generation to another” (Darwin to Romanes, 24 Jan. 1880; Darwin Life and Letters 105-06).[12]

As I suggested above, this theory of the evolution of instinct assumed that consciousness did not evolve, but was the condition of evolution itself. Moreover, this theory depended on a peculiarly anthropomorphic methodology, in which consciousness becomes the measure of the minds of animals. Rather than challenge Darwin on this front, Romanes instead formalized Darwin’s common-sense approach, one that amounted to a mind studying itself at its own origins. This had the effect—as C. Lloyd Morgan noted—of rendering instinct a species of intelligence. But for his anti-evolutionary fervor, Fabre might have rescued invertebrate psychology from this strange analogical loop by reinforcing rather than eliminating the divide between instinct and intelligence. Invertebrates, he maintained, had no minds, but rather than demean their intelligence, this fact exalted their instincts. Invertebrates were special not because they revealed (our) intelligence; they were special precisely because they didn’t.

Forel, however, arrived at his own invertebrate psychology, and his own methodology, by adhering to an evolutionist account of the origins of instinct while avoiding a priori assumptions about the existence of mind. He agreed with Darwin and Romanes that “instinctive automatisms” are “gradually acquired and inherited,” but, he claimed, there are further “secondary automatisms or habits which arise through the frequent repetition of plastic activities and are therefore especially characteristic of man’s enormous brain development” (Ants and Some Other Insects 12). In other words, the stuff of mind—“intellect, feeling, and will”—follows the same evolutionary path as habits: namely, “perfection through repetition.” Intelligence was therefore no special indefinable quality—no prime mover of evolution—but a kind of behavior akin to instinctive behavior. In this conclusion, Forel may have picked up where Darwin left off in his early notebooks on mind.

Thinking of intelligence as a kind of behavior comparable to instinctive behavior gave Forel the psycho-physiological justification for a comparative psychology based not on physiological brain similarities between species, but on behavior. In a statement reminiscent of Réaumur, Forel wrote that, from a morphological perspective, the brains of the anthropoid apes “are nearest to ours” and “present the closest relation in structure and working.” Meanwhile, the brains of humans and insects manifest dramatic differences: human brains have “more nervous substance” and “many more neurons” because our “plastic activities” (behaviors) require more complex physiology than the “automatic” behaviors of ants. But the manifestations of these different brains—that is, our behaviors—were of a piece. And, astonishingly, he wrote, “it is relatively inferior animals, the social insects, that exhibit a psychology nearest to that of man” (“Social Life of Ants” 564). Forel believed ants and other social insects to be as advanced in the development of their “automatic” instincts as humans are in the development of “plastic” intellect, an analogy that made them more psychologically familiar even than the apes.

As evidence, he cited the slave-making and cattle-keeping instincts of the ant Formica sanguinea, an example Darwin used in his discussion of instinct in the Origin. Forel saw no meaningful difference in human and ant when viewed from the level of complexity that allowed two different orders of life, vertebrate and invertebrate, to maintain slaves or cattle. At such extremes, “they resemble two terminal branches of a tree, but they may lead to similar results through so-called convergence of conditions of life” (Ants and Some Other Insects 13). This moment is important because it reveals a significant shift in the analogical function of invertebrates. For Darwin, as for Romanes, such behaviors provided analogical evidence for an evolutionary genealogy of mind. But Forel saw that convergent evolution could explain how two distinct phylogenies could still produce similar (i.e. analogical) behaviors, such as slave-making in ants and men. His own behavioral analogy did not therefore require positing mind in simpler forms of life in order to hypothesize an evolutionary genealogy of mind. By making intelligence a kind of behavior, Forel removed intelligence and consciousness as necessary conditions of both mind and the study of mind. Fabre had arrived at a similar conclusion, but at the expense of a comparative, invertebrate psychology. The minds of his insects provided no clue to anything but their own minds. For Forel, however, rather than rendering a comparative psychology of ants and men insupportable, shifting from an evolutionary analogy to a behavioral one provided the very grounds of such a psychology.

The Language of Mind

Underlying Forel’s psychology lay a challenge to the premise of modern psychology that would claim that consciousness is the true basis for mind. Though psychologists have traditionally understood consciousness in some form as a necessary condition of mind, Forel claimed that consciousness “does not exist as such.” Instead, it is a “reflex” of “brain-activity” (Ants and Some Other Insects 5). Consciousness only appears to us, “subjectively,” as a “summary synthesis” that “grows more summative and more synthetic” as we rise to higher and higher abstractions. To give my own analogy, consciousness is like a mapmaker that comes to see his maps, not as representations of on-the-ground realities, but as abstract artworks in and of themselves, as compositions of color and form and line that gain in power to summarize details until map is no longer territory. While from the height of the mapmaker’s abstractions, the whole map appears as a single unit, it is, in fact, just a “patchwork full of contradictions.”[13]

What this means, he thought, is that we are indecipherable to ourselves. But unlike Sigmund Freud, who would soon arrive at a similar conclusion, Forel believed that a psychology premised on conscious introspection is faulty. To study the mind from within its own abstractions relies on the very illusion that Forel saw as a function of brain physiology. The mind cannot study itself. And because language, our subjective self-reporting of our mental state, merely indexes consciousness, Forel advanced instead a psychology of behavior. Behaviors “betray [our] true inner being better than […] spoken language.” Since we share behaviors with the animals, their “attitudes and behavior […] have for us the value of a ‘language,’ the psychological importance of which must not be underestimated” (6).

There could be no greater rebuttal to Darwin’s common-sense analogy or Romanes’s “ejective” comparative psychology than Forel’s challenge to the very idea that we are experts in our own mind. Forel’s psychology was based on a powerful analogy: that animal behaviors speak the true language of mind. They are a kind of lingua franca, a universal language. A true comparative psychology would therefore make ourselves known to ourselves not, as Romanes had it, by reference to our own subjective experience, but rather by reference to the psychology of animals. The behaviors of ants, in particular, Forel thought complex enough and near enough to our own to provide a language rich in psychological detail. And so where Fabre employed the idea that insects are “documents of inestimable value” for a “universal psychology” in a metaphorical sense, Forel’s ants were literal documents to be read.


Forel’s discovery of behavior as a universal language of mind sent him on a further quest to discover, through experiment, the grammar of this language. He sought the ant’s minimum psychic phenomena, the smallest unit or quanta of mind that would allow for comparison across species. He called this unit a “psychome,” and it might remind us of the phoneme in linguistics, the smallest unit of a word that would differentiate its meaning from another word. For example: the “m” sound in “mat” distinguishes the word “mat” from “cat.”[14]

Forel inherited from the sensationalists a belief in the centrality of the senses in connecting mind and brain, as well as a belief that the senses were common across species. By removing the senses of the ant one by one, he hoped to find the minimum of mind rooted in what he considered its fundamental sense. Ants don’t possess hearing in any meaningful degree, and their eyesight is too poor to be of much use. But their sense of smell is remarkably advanced, and in this he finds the key to their psychology.

Ant smell receptors reside in “the club-shaped flagellum” at the terminus of their antennae, which they can move around independently. As a result, the ant “possesses two properties which are lacking in the vertebrates.” First, they smell by touching, and second, smell is essential to their perception of space. By touching things as they move along, ants produce an “odor-image” that allows them to create memories of spatial relationships (Ants and Some Other Insects 43).

Forel calls the ant’s synthesis of space, smell, and memory its “topochemical” sense. This sense makes up the ant’s image of its world: call it the ant’s psychic “world-picture.” Remove the antennae and you remove the ant’s ability to orient itself “on the ground.” But the topochemical sense also forms the basis of the ant’s social world: and so remove the antennae and you also “destroy [its] power of distinguishing friends from enemies” (16). It was the complexity of ant society that in Forel’s view made ant psychology comparable to humans, and so the topochemical sense is the foundation for any comparative psychology with it.

Any language of comparison is governed by the grammar of this sense. We might not possess this specific “topochemical sense,” but we too can smell and touch and remember. This analogical sense-affinity is enough, he thinks, to run the following thought experiment:

I would beg you to hold fast to what I have said and then to picture to yourselves an olfactory sense, i.e., a chemical sense effective at a distance and like our sense of smell, capable of receiving impressions from particles of the most diverse substances diffused through the atmosphere, located not in your nostrils, but on your hands. For of such a nature is the position of the olfactory sense on the antennal club of the ant.

Now imagine your olfactory hands in continual vibration, touching all objects to the right and to the left as you walk along, thereby rapidly locating the position of all odoriferous objects as you approach or recede from them, and perceiving the surfaces both simultaneously and successively as parts of objects differing in odor and position. It is clear from the very outset that such sense-organs would enable you to construct a veritable odor-chart of the path you had traversed. (42-43)

This “contact-odor chart” would provide “the accurate odor-form of the objects touched” in the form of “round odors, rectangular odors, elongate odors,” even “hard and soft odors in combination with the tactile sensations.”

Forel believed that the topochemical sense was “no enigma, but on the contrary a necessary psychological postulate” (44). It is the ant’s “psychome,” the smallest and most essential unit of its psychology. It is unique or almost unique to ants. Therefore we can isolate the essence of ant experience—or, what it is like to be an ant—in its topochemical sense. The ultimate payoff of Forel’s thought experiment is to build an analogy between our two species in part by combining two of our senses, smell and touch. This analogy relies on two important qualities: first, our sense affinity with other forms of life; and second, our imagination, which he considered the “loftiest and finest expression” of our minds. We can, he thought, imagine combinations like round odors and soft odors. Comparative psychology thus lay at the intersection of imagination and instinct.

The Sad Afterlife of Invertebrate Psychology

In his concluding remarks to a chapter on “Problematical Organs of Sense” in his On the Senses, Instincts, and Intelligence of Animals with Special Reference to Insects (1889), John Lubbock, the entomologist and Darwin’s neighbor and frequent correspondent in map iconKent, addressed the special challenges to any scientific understanding of the relationship between sense and psychology in invertebrates. He referred to these challenges under the rather mysterious phrase “the unknown world,” characterizing what I have called the black box, or the minds of invertebrates. Among the “problematical organs” he includes such perplexing sensory apparatuses as the nerves of some “lower animals” that confound our notion of what a sense is, such as in the case of those nerve endings that “terminate on reaching the skin at the base of rod-like structures similar […] to the rods of the retina, or to the auditory rods of the ear”; or the “eyes” of leeches, which likewise seem to be related to touch; and the sensory hairs of the Medusae, which “in all probability, serve as an organ of sense, but what impressions they convey it is impossible to say” (187). Such features, he says, represent the limits of objective analysis. Despite the advances of our most powerful instruments for seeing, or in fact for slicing up the brain, he notes, we simply cannot comprehend such structures as eyes that feel, or skin that hears and sees. These sorts of curiosities defy objective analysis. Look as we might for evidence of their function in even the minutest physiological structures, “even […] microscopes far more powerful than any we now possess [would] not enable us to obtain by direct vision any idea of the ultimate molecules of matter” that make up these perplexing structures (191).

But this objective limit, in contrast to Forel’s thought experiment, also confounds our ability to imagine what the world must be like to these organisms—that is, to use Romanes’s formulation, the quality of their conscious experience. Lubbock writes rather poetically of this limit: “The familiar world which surrounds us may be a totally different place to other animals. To them it may be full of music which we cannot hear, of color which we cannot see, of sensations which we cannot conceive.” As if in direct response to Romanes’s “eject,” Lubbock writes, “We have five senses, and sometimes fancy that no others are possible. But it is obvious that we cannot measure the infinite by our own narrow limitations” (192). Where Darwin, Romanes, and Forel all saw human senses as the standard of measurement for the psychology of invertebrates, Lubbock believed we cannot measure the experience of other organisms by these senses. The mental differences that must exist due to differences of physiology cannot be overcome by analogy, nor by imagination. To Lubbock, invertebrate psychology represented a radical displacement of the mind of man. Nevertheless, he says, the limit of our affinity with invertebrates represents “the true interest of natural history.” That is, not “stuffed birds and beasts in glass cases,” “insects in cabinets,” or “dried plants in drawers”, but “their relations to one another,” “their instincts and intelligence,” and “what the world appears to them” (192-93), despite that he saw no method for a way forward. Philosophical natural history indeed.

Lubbock essentially denied the possibility of an invertebrate psychology—not, like Fabre, because he denied that invertebrates possessed a quality of mind analogous to our own, but because he saw such a psychology as the limit of inquiry. He did not deny that spineless things possess experience, but he believed the quality or nature of that experience to be beyond our comprehension. Lubbock therefore represents a detractor to what might have been an emerging discipline, pioneered by Darwin, Romanes, and Forel, premised on the belief that the minds of invertebrates are knowable. Each of these would-be psychologists saw connections between the mind of man and invertebrates. Whether through an evolutionary analogy, as Darwin thought, through the undefined and undefinable quality of our own conscious experience, as Romanes thought, or through common behaviors rooted in a minimum of mind, a psychome, as Forel thought, “there is,” they all agreed, “such a thing as comparative psychology” (Forel, Ants 35). Their optimism reflects a nineteenth-century belief in the power of analogy to build connections between unlike things—a belief galvanized, perhaps, by Darwin’s release of nature and science from the binds of theology. Mind, they thought, might flow through even the smallest channels of life. However, the twentieth century challenged the idea that science or analogy can draw us closer to our spineless distant cousins and proved Lubbock prescient. The reasons for this lay beyond the scope of this analysis, but I will conclude with one further thought experiment from the philosopher of mind Thomas Nagel’s classic 1974 essay “What Is It Like to Be a Bat?” in order to gesture at the sad fate of invertebrate psychology, as well as at the consequences of this fate.

Nagel’s essay has become a standard reference in any account of mind in nonhuman animals. He set out to find the limits of scientific analysis when it comes to mind. The question of his title is the central question of comparative psychology: Do other forms of life have experience of the world? If so, what is the quality of that experience? And how can we know? He shares with Erasmus Darwin and his successors the premises that “mind” is the product of the physiology of brain and that brain physiology is a function of the senses. The senses provide the stuff of mind because they determine the architecture of brain.

Equipped with these identical premises, Nagel ran a thought experiment that produced very different results. Bats hang relatively close to humans on the tree of life. We share a common ancestor that existed only about 80 million years ago. We are sufficiently similar to bats to believe that they do in fact have experience of the world: there is something it is like to be a bat. (If you disagree, consider that we are more closely related to bats than to dogs.) Nagel calls this the “subjective experience” of the bat, or, what the world must feel like to that organism. But bats possess a sense we do not: echolocation. If there is something it is like to be a bat, then echolocation is it. Echolocation makes bat experience bat-like; and while we can, he thinks, imagine what it would be like for us humans to build a world-picture with sound, we cannot imagine what it is like for a bat to experience that picture. Our shared physiology does not extend so far as a bat’s ability to produce sound-pictures. And so ultimately the subjective experience of nonhuman animals cannot be “expressed in [the] objective terms” of science. Subjective experience is the limit of scientific analysis.

Nagel dismisses analogy as an effective tool for overcoming this limit: he says analogies between senses, “for example, ‘Red is like the sound of a trumpet’ […] are of little use. That should be clear to anyone who has both heard a trumpet and seen red.” But perhaps more revealing than Nagel’s dismissal of analogy is another, less obvious dismissal. Nagel claims that he has “chosen bats instead of wasps […] because if one travels too far down the phylogenetic tree, people gradually shed their faith that there is experience there at all” (438, emphasis added). In other words, Nagel’s essay might just as well have been called “What Is It Like to Be a Wasp?”. In 1974, less than a hundred years after most of the explorations examined here, the idea that a wasp—an invertebrate of the Hymenoptera, the order which includes the famously intelligent and social ants and bees—has experience at all, was unthinkable, even in a thought experiment.

There is, it seems, no such thing as an invertebrate psychology. But why does this matter? Invertebrates dominate life on earth by orders of magnitude, but, as Lubbock thought, we might as well exist on different planets. Maybe for this reason they seem utterly indifferent to our existence, even unaware of it. They do not, as the invertebrate psychologists believed, reflect back to us our own minds, and so do not satisfy our desire to find ourselves in nature. They have become, as Elias Canetti wrote, “outlaws.” We’ve relegated them to an ethical outland, murdering them in untold numbers in the name of pest control and science, in houses tented for termites and genetics laboratories thick with fruit flies. We exploit them unthinkingly for industry and agriculture. “The destruction of these tiny creatures is the only act of violence which remains unpunished even within us. Their blood does not stain our hands, for it does not remind us of our own” (qtd. in Raffles 121). Perhaps it is going too far to attribute the absence of ethical regard for invertebrates to the erosion of a nineteenth-century faith in the analogy of invertebrate minds to ours—after all, Romanes was a strong proponent of vivisection, as were Darwin and Forel. But as historians and critics of science have reminded us, words and the structure of language are more than just ways of talking: they reveal ways of thinking. Modern science, in its quest to free itself of analogies that entangle us in philosophical or ethical issues through a language at once “correct, scientific, abstract, hygienically pallid” (Nussbaum 19), in fact “imprisons us” in an “intellectual monoculture” that objectifies nature (Kimmerer 55). Nineteenth-century invertebrate analogies reveal a brief episode in the history of scientific thought before the structures of objective, and objectifying, thought prejudiced us against the possibility of imagining a place in our lives beyond utility for the lives of spineless things.

published January 2017

Bryan B Rasmussen is Associate Professor of English at California Lutheran University, where he specializes in the literature and history of natural history. Ongoing projects include research in the history of invertebrate psychology, science and self-writing, and early-twentieth-century scientific expeditions in Southern California and the Baja Peninsula. He is a former Charlotte W. Newcombe Fellow in Religion and Ethics (Woodrow Wilson Foundation) and has served as Managing Editor of the journal Victorian Studies.


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[1] See Farber, Finding Order, ch. 1, for a discussion of Linnaeus’s system as an “artificial” one, and for the challenge offered by his contemporary Comte de Buffon. Buffon proposed a “natural” system that “went beyond particulars” like sex characteristics, “to construct an overall picture of the order of nature” (15), which led him to deemphasize classification as the primary task of the naturalist in favor of identifying larger patterns, such as historical connections among species (21).

[2] See, for example, Young, who argues that “psychological theories lay at the every basis of much of evolutionary theory” (69). Young considers evolutionary theory a kind of “applied psychology” that took reigning ideas about mind and behavior, from physiology to Utilitarianism to social science, and gave them firm grounding in the natural world.

[3] For a lengthy treatment of Darwin’s early reliance on a use-inheritance model of species change, see Richards, 71-126.

[4] See Richards, 71-74 for another interpretation of Darwin and philosophy. To regard Darwin as coming out against philosophy, says Richards, risks turning him into a Neo-Darwinist—that is, it risks reading contemporary interpretations of Darwinian theory backward onto Darwin himself. But Richards masterfully shows the ways in which this is a caricature. I agree with Richards, but nevertheless, think that Darwin punted the question of the origins of mind. I further think that Darwin did come to regard his own theory as perpetrating a “grossly utilitarian” view of nature—a sentiment he left unpublished in his chapter on Instinct, and which left, perhaps, little room for mind in nature.

[5] Young is careful to separate the “implications” of Darwin’s work for psychology from Darwin’s own work, which was that of a field naturalist and geologist (59).

[6] Darwin himself was suspicious of analogy, which may tell us something about why he chose not to pursue the question of mind. As he wrote in Origin, he hoped that “terms used by naturalists of affinity, relationship,” etc., will one day “cease to be metaphorical, and will have a plain signification” (485). Analogies, he thought, smacked of magical thinking: “They could claim more than they proved” (qtd. in Beer 75). And so he sought, writes Beer, “true affinities” that would “move beyond the provisional and metaphorical” (76). Perhaps one result of this attitude toward analogy and metaphor is that the relationship, the affinity, of the mind of man and the mind of the worm remained uninterrogated.

[7] The example of the chick for the demonstration of instinct was so common the comparative psychologist C. Lloyd Morgan dubbed it “the philosopher’s chick” (Introduction xi). See also George Mivart, “Organic Nature’s Riddle.” Fortnightly Review 43 (1885).

[8] Psychologists would now call this “theory of mind”: using mental models made up of our own first-person experience of our minds, we can “read” the minds of others.

[9] Romanes actually used the phrase “lapsed intelligence” (see for example, Mental Evolution 178, 271).

[10] For a thorough but slightly different treatment of Romanes on the idea of mind in nature, see Richards’s important discussion, 363-70.

[11] See again Young, who argues that spiritualism was bound up in Monist philosophers’ desire “to bridge the gaps between mind and body” (77). There is evidence that suggests that Monists’ interest in mind beyond the brain signals a late-century return to a Romantic sensibility, which sought some quality of “will” or agency or “force” in nature beneath the level of material processes.

[12] See Mivart on this oft-cited example. See also Romanes in Animal Intelligence (16-17); and Fabre’s rebuttal to this idea in The Wonders of Instinct.

[13] I am reminded of Herbert Spencer’s account of the origin of consciousness in Principles of Psychology (1855): “In the development of mind there is a progressive consolidation of states of consciousness. States of consciousness once separate become indissoluble. Other states that were originally united with difficulty, grow so coherent as to follow one another without difficulty. And thus there arise large aggregations of states, answering to complex external things—animals, men, buildings—which are so welded together as to be practically single states. But this integration, by uniting a large number of related sensations into one state, does not destroy them. Though subordinated as parts of a whole, they still exist” (588-89).

[14] Not for nothing, perhaps, did Forel, elected to the Swiss Natural History Society, share company with the entomologist Henri de Saussure, father of structural linguist Ferdinand, who elaborated the idea of the phoneme.