Pests,plagues,pleurites,and pébrine: The history of invertebrate pathology from antiquity to 1900

Falstaff: “I will not lend thee a penny.”

Pistol: “Why then, the world’s mine oyster, which I with sword will open.”

—William Shakespeare (1602), “The Merry Wives of Windsor”

This short account cannot do justice to the long and rich history of the genesis and evolution of invertebrate pathology. The emphasis in the succeeding text, therefore, is to draw attention to the early dawning of interest in the lives—and in the deaths—of “les petites bêtes” (as the French entomologist Jean-Henri Fabre [1823–1915] termed them) and to summarize, with examples, advances in knowledge over the centuries that led to the emergence of the discipline of “invertebrate pathology” as we know it now. As the following text illustrates, the subject did not evolve spontaneously. Its growth mirrored the history of other forms of pathology whereby initial studies on anatomy and physiology, often supplemented by behavioral observations, led to an understanding of the causes and mechanisms of disease in a wide range of taxa.

Prehistory

For thousands of years, long before the advent of written records, Homo sapiens would have been aware of invertebrates. Some species were domesticated for economic and social reasons, such as the honeybee (Apis mellifera) and the silkworm (Bombyx mori).^4,39,49,50 Early humans would have observed instances of disease and death in these and some other taxa even if they did not understand the causes. The Chinese recorded diseases of the silkworm nearly 5000 years ago. It is possible that such conditions were familiar also to scholars during the period from 2350 to 900 BC, when publications first appeared on species such as the elephant. ²⁷

Fluctuations in numbers of economically free-living swarming insects must also have been noted. An example would have been the extensive swarms of “kungu” (lake flies), Chaoborus edulis, still seen in East Africa, which for millennia have provided local communities with protein, but which were not documented until the arrival of Europeans. ³⁴ Better chronicled were locusts, referred to in both the Bible and in the Quran, and the honeybee. The life and habits of the latter are used to signify to Muslims the great works of Allah.^9,50,51

Classical Antiquity

Classical antiquity is usually defined as the period between the eighth century BC and the sixth century AD. It centered on the Mediterranean Sea and comprised the civilizations of the Graeco-Roman world—ancient Greece and ancient Rome. A useful account of insects and other invertebrates in this era was provided by Beavis who argued that research on “classical entomology” had been sadly neglected. ⁴ He discussed not only the identity of the various invertebrates recorded by classical writers, but also such matters as their relations with man (sic) and their alleged medical uses. Other relevant books were by Davies and Kathirithamby ²⁵ and the German text Antike Tierwelt. ³⁹

Aristotle (384-322 BC) is generally considered to be the founder of biological science. ⁵ His Historia Animalium, written in the fourth century BC, was probably the most influential zoological text in classical antiquity. In it, he offered a comparative survey of internal and external body parts, reproductive methods, embryogenesis, feeding and breeding habits, and hibernation. Although Aristotle concentrated on what he called “blooded animals” (vertebrates), the 500 species that he described included some shellfish and insects. He documented many accurate eye-witness observations of animals, including the ability of the octopus to change its color and its possession of a sperm-transferring tentacle. Historia Animalium had a profound influence on zoological thinking. It remained a primary and respected source of knowledge until the 16th century when a new generation of European investigators recorded their own observations.

Three centuries later, Gaius Plinius Secundus (23/24–79 AD), also known as “Pliny the Elder,” was a naturalist, author, philosopher, and military commander in the early Roman Empire. ⁵ Pliny wrote “Naturalis Historia” (Natural History), which was noteworthy on many accounts, including the breadth of its subject matter, its reference to original authors, and the inclusion of a comprehensive index. Pliny recorded many matters relevant to the health of invertebrates, including a description of brood diseases of the honeybee. Classical authors referred frequently to the adverse effects that some invertebrate animals could have on humans. ⁵ Many alluded also to the alleged medicinal uses of certain species. Pliny was among those who stated that spiders’ webs could staunch the flow of blood and, therefore, be used to treat wounds—a forerunner of current scientific interest in this product. “Naturalis Historia” is, unfortunately, the only work by Pliny to have survived. He died in the 79 AD eruption of Mount Vesuvius that destroyed the cities of Pompeii and Herculaneum. Perhaps rather appropriate in respect to Pliny’s studies, mosaic recovered from the Pompeii remains include images of an octopus, a squid, and crustaceans.

Pests affecting beehives attracted the attention of other writers as well. ⁵ The poet Virgil, Publius Vergilius Maro (70–19 BC), described spiders spinning webs over hive entrances to capture bees. Other authors appeared to confuse spiders’ webs with those spun by the larvae of wax moths—pests that lay their eggs inside beehives.

Medieval Period

The term “Dark Ages” is sometimes used to refer to the Early Middle Ages in Western Europe, which began with the fall of the Western Roman Empire and lasted approximately from the fifth to the late 15th centuries. ⁵ Although characterized by Western cultural and economic decline, Islamic study and writings provided continuing influence. The Persian philosopher Avicenna wrote his Canon of Medicine, which was to become the standard human medical text. Important contributions to our knowledge of invertebrates were made by the Muslim theologian and author AbūʿUthmanʿAmr ibn Baḥr al-Kinānī al-Baṣrī, commonly known as al-Jāḥiẓ (776–868/869 AD). His best-known publication was the Kitāb al-Ḥayawān (The book of living). While some of his descriptions are allegorical or symbolic, it is clear that al-Jāḥiẓ was a keen observer. He wrote that mosquitoes “know instinctively that blood is the thing which makes them live” and that when they see an animal, “they know that the skin has been fashioned to serve them as food..”

The medieval period progressed into the Renaissance and the Age of Discovery, discussed below and extensively in Cole. ⁵ The Italian polymath Leonardo da Vinci (1452–1519) born in the 15th century is relevant to the transition referred to above because he was the pathfinder as far as comparative studies on animals were concerned.

Modern Period

The Modern Period can be considered to span the 350 years from the Enlightenment, the “Age of Reason” in the late 17th century, which was characterized by rigorous debate and discovery. They were exciting but often dangerous times when scientific research gathered momentum and broke free from earlier religious, philosophical, and political constraints. ⁵

As far as invertebrates were concerned, the 17th century in Europe saw a more scientific approach, with particular emphasis on anatomy. It is important to understand the significance of such apparently basic studies. Little was known about the structure of small animals, especially invertebrates, and until the advent of genetic techniques such as DNA sequencing, comparative morphology was the primary route to comprehending phylogeny.

Much of the literature about comparative anatomy produced during the Modern Period was in languages other than English—initially Latin, then in French, German, Dutch, Russian, and other European tongues. ⁵ Despite this, many modern North American publications fail to mention, let alone refer to, books and articles in languages other than English. This is a big mistake if one is to plot invertebrate research. Indeed, important works were still being published in French and German only 30 years ago ¹⁰ —some still are—and there remain many publications in Russian and other Eastern European languages, written before the fall of the “Iron Curtain,” that continue to be ignored by western scientists.

Space does not permit a detailed discussion of the numerous persons in Europe who studied animal structure. Many focused on vertebrates, but all contributed to a better understanding of similarities and differences in the anatomy of disparate species. For more information, the reader is referred to the seminal text by Cole. ⁵

The French played an important part in comparative anatomy. Baron Georges Cuvier (1769–1832) was a naturalist and zoologist and helped establish comparative anatomy and paleontology as bona fide disciplines, expanding Linnaean taxonomy by grouping classes into phyla and incorporating both fossils and living species into a classification system. Cuvier was primarily concerned with vertebrates, but his 1817 publication The Animal Kingdom Distributed according to Its Organisation described the classification of arthropods and segmented worms, molluscs, and the Radiata.

The microscope was invented in 1609 by Galileo di Vincenzo Bonaiuti de’ Galilei (“Galileo”) (1564–1642), but early versions were poor; there was only one lens which had to be placed close to the specimen. ⁵ Illustrations of microscopic structure of insects started to be published from about 1625 with Robert Hooke’s (1635–1703) classic Micrographia appearing in 1665. Antonie Philips van Leeuwenhoek (1632–1723), a businessman and scientist during the Golden Age of Dutch science, is often considered the “father of microscopy.” ⁵ He examined more than 200 species of animal, from “Infusoria” (minute freshwater organisms—the term is now obsolete), insects (Fig. 1a), and arachnids to whales. He described the dissection of spiders in one of his letters in 1673. These include an egg removed from a parent and dissections of larvae

Figure 1.

(a) Drawings by Leeuwenhoek, 1704, of his studies on cochineal. Various features of a scale insect (probably the species that is now known as Dactylopius coccus). (b) Swammerdam’s drawing of the compound eye of a honeybee, showing remarkable detail and recognition of the complexity of the organ. Swammerdam described minute tracheae penetrating the eye, the packing of pigment, and the characteristic elongated crystalline cones, some of which are visible in the figure. (c) Drawing by Nicholls 1730 of a gynandromorph lobster. The right side shows female organs, the left male. Various features confirm the diagnosis, such as the different locations of the genital apertures, the disparate appearances of the first abdominal appendage, and the breadth and hairiness of the female abdomen in contrast to that of the male.

From an early stage, the eyes of invertebrates attracted interest. ⁵ In 1625, Francesco Stelluti (1577–1652) published a description and a figure of the compound eye of the honeybee. The Italian surgeon and anatomist Marco Aurelio Severino (1580–1656) is sometimes denigrated because of his mystic speculations, but he is relevant to invertebrate pathologists because he dissected molluscs, crustaceans, isopods, crickets, beetles a “looper” (geometrid) caterpillar, a scorpion, and a spider.

Marcello Malpighi (1628–1694), after whom the Malpighian tubules of insects and arachnids are named, studied and drew various animals, including invertebrates. He was another polymath, but he faced opposition to his work from the medical community. ³⁶ Malpighi was the first to realize that insects breathe through their tracheae. He demonstrated that if a silkworm was bathed in oil it “immediately had convulsions and died.” In 1669, he published his Dissertatio epistolica de bombyce. ⁴⁸ Malpighi’s Bombyx is still preserved in the library of the Royal Society in London. Previously, Andreas Libavius (1550–1616) found the heart of a silkworm in 1599, but he did not recognize it as such despite its pulsations, leaving Malpighi to confirm its identity. ⁵ Malpighi’s contemporary, Jan Swammerdam (1637–1680), was a Dutch biologist and microscopist. He was the first to illustrate that the various instars of an insect—ovum, larva, pupa, and adult—are forms of the same creature. ⁵ Swammerdam was inspired by Malpighi but was able to correct some of the latter’s errors (Fig. 1b).

Scientific investigation of the morphology of spiders dates back nearly four centuries. The English naturalist and physician Martin Lister (1639–1712) published his Tractatus de Araneis in 1678. In addition to his arachnological endeavors, Lister showed that hibernating snails have a slow, faint, pulsation of the heart. He dissected both snails and slugs and was able to correct many of the errors of Redi Francesco Redi (1626–1697) {often described as the “founder of experimental biology”}. The medical anatomist Frank Nicholls, physician to George II, (1699–1778), warrants a special mention in this Commentary, because in 1730, he reported on his dissection of gynandromorph lobster (Fig. 1c). ⁵⁸

In any assessment of the evolution of invertebrate pathology, it is vital to understand that the investigation of these animals was at first greatly hampered by the difficulty of preserving them. ⁵ As Nehemiah Grew put it “Worms caterpillars and other soft insects . . . shrink up so as nothing can be observed of their parts after they are dead.” ³³ The situation began to change in the 17th century when several scientists reported satisfactory preservation of both vertebrate and invertebrate animals in “spirit of wine.” As early as 1670, Swammerdam was reported to employ this product to preserve insects, and by 1710, Leeuwenhoek was routinely keeping his young oysters in spirit of wine.

Scientific advances based on anatomy and physiology continued into the 18th century and increasingly led to a better understanding of disease and recognition of pathological processes. Perhaps, the greatest luminary of that period was John Hunter (1728–1793), remembered as a surgeon, a comparative pathologist, and as one of the founders of Britain’s first veterinary college (1791). Hunter had been a naturalist since childhood and summed up in his own words as follows “When I was a boy, . . . I watched the ants, birds, bees, tadpoles and caddis worms; I pestered people with questions about what nobody knew or cared anything about.” He applied the same powers of observation to his studies on humans and other animals. His museum in London, although badly damaged in the Second World War, still includes invertebrate material such as a mounted specimen showing a healed shell in a bivalve. ¹¹

It was, however, the 19th century that heralded a real understanding of the nature of infectious disease in invertebrates as well as vertebrates. It is generally accepted in the English-speaking world that the study of insect diseases as a subject in its own right was first mooted in a chapter in the seminal text by Kirby and Spence. ⁴² The two biggest names in invertebrate disease studies in the 19th century—largely on account of their epic studies on the silkworm – were probably Agostino Bassi, “the father of insect pathology,” ¹⁶ and Louis Pasteur (1822–1895),^3,49,59 both Frenchmen.

Pasteur’s initial contribution to invertebrate pathology concerned the microsporidian disease known as “pébrine,” and in his Études sur la Maladie des Vers à Soie, he also described “flacherie.” ⁵⁹ Pasteur’s discoveries undoubtedly saved the French silk industry and what he described in his silkworms were the first demonstrated microbial diseases of animals. The 19^th century can rightly be called the renaissance for insect pathology. It is interesting to note that Pasteur, a chemist, had never seen a silkworm until he was introduced to them by Jean-Henri Fabre, “the father of entomology.” Fabre himself contributed to invertebrate pathology. For instance, he studied the parasitism of the butterfly Pieris brassicae by braconid wasps Microgaster, which included the performance of autopsies on affected larvae. Fabre’s greatest claim to fame, however, is that he introduced behavioral studies into scientific research on invertebrates. ²⁹

Marsden recently provided a useful review of Pasteur’s work, emphasizing how a disease problem in insects can be successfully tackled using scientific logic and experiment, ⁴⁹ but over a century earlier, Émile Duclaux (1840–1904) had written ecstatically:

. . . Pasteur, at the conclusion of his researches, found that he had not only solved the problem which he had set himself of the revival of sericulture, but had also placed upon an experimental basis the great questions of contagion and heredity which dominate the whole of pathology. ²⁸

Bassi was a microbiologist and chemist. For much of his career, he was associated with the work of Louis Pasteur, with whom he not only collaborated (Bassi was the first to show that a fungus caused disease in silkworms), but also took part in experiments to disprove the theory of spontaneous generation. In the 1870s, Bassi studied Phylloxera vastatrix (now called Daktulosphaira vitifoliae), a hemipteran, originally native to North America, that is a pest of commercial grapevines. He and Pasteur recognized the potential for using organisms to control insect pests. Fungi and protozoa tended to be the main focus of attention in respect of invertebrate disease in the 19th century, but within a few years, the French microbiologist Félix d’Hérelle (1873–1949) had opened up a whole new area of research with his use of pathogenic organisms to control locusts and as a co-discoverer of bacteriophages.

In the 19th century, amateur naturalists were among those who observed, recorded, and often drew signs of parasitism and apparent infection in invertebrates. Molluscs attracted particular interest in Europe. Those participating in these studies were often amateur naturalists, among them several women. They regularly recorded pathological changes in shells. ⁷ There were also studies on diseases of captive butterflies. Entomologists who bred Lepidoptera for study or sale were very aware of the many threats to the health of their charges, ranging from parasitic wasps and flies to hypothermia. ⁵⁷ This led later to research by far-sighted entomologists such as Brian Gardiner ³² and Claude Rivers ⁶⁴ who showed that a whole spectrum of micro-organisms could affect butterflies, including bacteria, fungi, protozoa, and viruses. A door to invertebrate pathology studies had opened and an approach that could contribute to species conservation rather than justpest control.^16,23

Fungal diseases were documented early in this period, probably reflecting the ease with which many of these afflictions could be recognized, even with the naked eye. A late 19th-century work by Cooke ⁶ detailed fungal infections of insects and included illustrated drawings of hosts with fungal bodies attached (see Fig. 2a, b). Interest grew in the parasitization of insects by fungi, and many scientists contributed to this growing field of study. Among them was Élie Metchnikoff (1845–1916), who in 1870 performed experiments on Metarhizium anisopliae in the beetle Anisoplia austriaca and in so doing paved the way for the search for other organisms that might be capable of killing injurious insects. The work of Metchnikoff in invertebrates also contributed to the understanding of human and vertebrate animal pathology. For example, he demonstrated the ingestion of foreign material by cells using invertebrates by discovering that certain cells had surrounded and engulfed the splinters placed in the bodies of the starfish larvae (Fig. 2c). He wrote “Dans tous les cas la lésion fut suivie d’une accumulation phagocytes mésodermique . . ..” He called the cells “phagocytes” (Greek—“devouring cells”), and he named the process phagocytosis. It was a process that was to be his subject of research for the next 25 years. ⁵⁵

Figure 2.

(a) The fungus Cordyceps unilateralis on the body of an ant from Brazil (After Cooke)}. (b) The fungus Cordyceps sphecocephala on a wasp (After Cooke). (c) One of Metchnikoff’s original drawings showing “phagocytes” attracted to a foreign body in a starfish. (d) Drawings by Elkan of one of his many step sections of a normal Portuguese oyster Crassostrea angulata.

The 19^th century had also seen the emergence of scientific bodies focused on certain taxa. The Royal Entomological Society is one example. It was founded in 1833 and among its earliest Fellows were both Alfred Russel Wallace (1823–1913) and Charles Darwin (1809–1882). Both Charles Darwin and Alfred Russel Wallace were keen observers of invertebrate behavior and were probably influenced by Fabre. Darwin was particularly fascinated by earthworms, and they were the subject of his final book. ²⁴ The Royal Entomological Society publications today cover topics of relevance to invertebrate pathology including agricultural and forest entomology, physiological entomology, molecular biology, and medical and veterinary entomology. Like its counterparts in other parts of the world, membership of the society includes scientists from various disciplines with a shared interest in insect infections and immunity.

Specific involvement by veterinarians in the diagnosis and study of insect diseases can perhaps be traced back to another giant of the early 20^th century, Sir Arnold Theiler (1867–1936), the first Director of the Onderstepoort Veterinary Research Institute in South Africa. In 1899, Theiler was consulted about the locusts that were ravaging southern Africa, prompting him to investigate a fungus that appeared to be capable of killing locusts. Theiler recorded how useful it was in these investigations to recall the diseases that had afflicted his father’s honeybees. ³⁵

Edward Elkan (1895–1983), a medical doctor who fled from Germany to England to escape the Nazis, applied his skills in histology to the production of serial and step sections and line drawings of various taxa, many of which remain in the Edward Elkan Reference Collection, held by the author (JEC). An example was his micro-anatomical studies on the Portuguese oyster, Crassostrea angulata, which was decimated by iridoviral disease in the 1960s, necessitating research on the pathology of the condition (Fig. 2d, Elkan E, unpublished report in the Edward Elkan Reference Collection). The work of Elkan heralded a movement away from the gross anatomical research on invertebrates outlined above to meticulous microscopy. This was to prove a boon to those battling with the pathological changes seen in invertebrates.^2,43,66 Countless contributions were to appear, in different European languages, especially but not exclusively relating to arachnid histology.^{20,30,41,43 –45,54,74} Edward Elkan collaborated closely with John Harshbarger in the United States and Peer Zwart in the Netherlands, and he corresponded in French with Gilbert Matz in France. All were to contribute greatly to our understanding of invertebrate pathology over subsequent decades.^{10,26,37,38,51 –53,79}

The dawn of the 21^st century provides a suitable point at which to start drawing this historical account to a close. The next 100 years were to see enormous advances in our understanding of invertebrate disease. Although the main focus was to remain orientated toward pathogens of relevance to pest control,^72,73 behind the scenes modest attempts were being made to understand how invertebrates kept for pleasure or commercial purposes might be kept healthy and to elucidate ways in which an understanding of the diseases and pathology of invertebrates might help conserve species rather than control their numbers. ³¹ Fields in which these advances were made included clinical treatment^{60,61,75 –77}; emergency care ¹³ ; anesthesiology ¹⁴ ; oncology^{15,37,38,51 –53}; hematology ⁶⁸ ; legislation ²² ; the management of invertebrates in laboratories,^8,78 including the use of species such as scorpions, ²⁰ spiders,^20,74 and leeches^9,69 as tools in medicine; the health of invertebrates in zoos and butterfly houses^18,19,21,56; the health of free-living butterflies, such as the North American monarch (milkweed) (Danaus plexippus)^1,46,70; the microbiota of insects and other invertebrates^61,62; host-parasite relations,^65,67,70 including the role of such organisms as Spiroplasma and Wolbachia; the effects of climate change involving, inter alia, bleaching and death of colonies of corals ⁶³ ; food hygiene, particularly in respect of shellfish and crustaceans; and the use of invertebrates to feed humans and livestock,^12,79 including wild birds. ¹⁷ In these and other endeavors, investigative pathology has played a pivotal role.

Captive invertebrate medicine, including pathology, truly came of age with the publication of Invertebrate Medicine, now in its third instar. ⁴⁷ The reading material outlined above was supplemented by relevant publications, most now online, from bodies such as the Veterinary Invertebrate Society (VIS) (veterinaryinvertebratesociety.wordpress.com).

Conclusions

It is clear that an interest in invertebrates, leading to a better understanding of their health, goes back centuries. Even William Shakespeare appears to have had some sympathy with invertebrates. In his play Measure for Measure, he wrote “The poor beetle that we tread upon . . . feels a pang as great as when a giant dies.” The belief that insects might feel pain is not a new one. The past few decades, however, have seen an explosion of enthusiasm for invertebrate pathology, prompted not only by the long-standing need for pest control but also by the growing demand, on both welfare and conservation grounds, to prevent and control disease in all invertebrates, both captive and free-living.

The most cheering aspect of contemporary invertebrate pathology is the involvement of scientists from many different disciplines—entomologists, malacologists, parasitologists, geneticists, biochemists, molecular biologists, conservationists, and both medical and veterinary graduates. This commentary is part of a focus issue of the journal Veterinary Pathology—a landmark in itself—and it is appropriate to remind readers that it took decades for veterinarians, whose training was essentially directed at domesticated mammals and birds, to venture out of their comfort zone and to respond to the challenges presented by diverse reptilian, amphibian, and piscine species. It is commendable that in recent years a few veterinarians, including the two editors and many of the contributors to this volume, have gone further and chosen to participate wholeheartedly in studies on the diseases and pathology of invertebrates—the taxa that constitute at least 90% of the animal kingdom.^40,47 It seems fitting to conclude with the salient part of the Shakespearean quotation with which this Commentary started—“The world’s mine oyster.” These four words remind us that, while an oyster may or may conceal a pearl, it is always worth investigating. Exciting opportunities in invertebrate pathology lie ahead.