Symbiosis (2016) 69:131–139

DOI 10.1007/s13199-016-0409-8

English translation of Heinrich Anton de Bary’s 1878 speech,

‘Die Erscheinung der Symbiose’ (‘De la symbiose’)
Nathalie Oulhen 1 & Barbara J. Schulz 2 & Tyler J. Carrier 3

Received: 20 December 2015 / Accepted: 22 April 2016 / Published online: 2 May 2016
# Springer Science+Business Media Dordrecht 2016

Abstract Die Erscheinung der Symbiose, meaning Bthe phe- 1 Introduction

nomenon of symbiosis^ in English or Bde la symbiose^ in
French, is a transcription of the 1878 lecture by the German Heinrich Anton de Bary (Fig. 1), addressed by students and col-
botanist and mycologist Heinrich Anton de Bary in which he leagues as Professor Anton de Bary or BThe Professor^, was born
first used the term ‘symbiosis’ in a biological context. De on 26 January 1831 in Frankfurt, Germany to August Theodor de
Bary’s speech was published in 1879 in German, later to be Bary, a physician with a keen interest in botany, and Emilie von
translated into French; though only fragments of his speech Meyer (Ahmadjian and Paracer 1986). In de Bary’s early years,
are available in English. Translating de Bary’s lecture is timely his father insisted he become a physician, and, in doing so, sent
because the field of symbiosis, especially with respect to mi- him to study medicine at Heidelberg University, Germany, and he
croorganisms, is expanding and the importance of symbiosis later transferred to the University of Marburg, Germany (Horsfall
is now recognized across the biological sciences. Researchers and Wilhelm 1982). While in medical school, de Bary researched
have now begun to sort through the early literature to uncover smut and rust diseases associated with cereals (field crops), which
original thoughts pertaining to symbiotic interactions. We be- at the age of 22 led him to publish a book titled, Untersuchungen
lieve that having de Bary’s lecture accessible to researchers in über die Brandpilze und die durch sie verursachten Krankheiten
English will help enhance interest in the history of symbioses, der Pflanzen mit Rücksicht auf das Getreide und andere
document de Bary’s pioneering contribution, and aid in estab- Nutzpflanzen (de Bary 1853; English translation: Studies on the
lishing an understanding for whom the lecture was intended smut fungi and the causes of plant diseases with respect to grain
and when biological symbioses were first recognized. We and other crops). In his book, de Bary sought, and succeeded, to
present a short biography of Heinrich Anton de Bary, a full disprove the dogma of spontaneous generation. In that same year,
translation of his lecture, and conclude by briefly highlighting de Bary received his medical degree with his dissertation titled, De
current endeavors in symbiosis research. plantarum generatione sexuali (English translation: The sexual
generation of plants).
Keywords Symbiosis . De la symbiose . Die Erscheinung der Following medical school, de Bary practiced medicine brief-
Symbiose . Heinrich Anton de Bary ly until deciding to make botany his primary subject (Horsfall
and Wilhelm 1982). Soon after, de Bary became an adjunct
lecturer (or ‘Privatdozent’ in German) at the University of
* Tyler J. Carrier
Tübingen Germany, where he assisted Hugo von Mohl, the
tcarrie1@uncc.edu German botanist and member of the Royal Society who coined
the term ‘protoplasm,’ or the living content of a cell
1
Department of Molecular and Cell Biology and Biochemistry, Brown encompassed by the plasma membrane. At 24, de Bary
University, Providence, RI 02912, USA succeeded Carl Nägeli, the Swiss botanist and chair of
2
Institute of Microbiology, University of Braunschweig, Botany at the University of Freiburg (Germany) who, perhaps,
Spielmannstraße 7, 38106 Braunschweig, Germany was most remembered for discouraging Gregor Mendel from
3
Department of Biological Sciences, University of North Charlotte at continuing to investigate inheritance in plants (Sparrow 1978;
Charlotte, Charlotte, NC 28223, USA Horsfall and Wilhelm 1982).

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132 N. Oulhen et al.

publications, but also completing several books, and describ-

ing six genera (Aphanomyces de Bary, Aplanes de Bary,
Echinostelium de Bary, Phytophthora de Bary, Piptocephalis
de Bary, Pythiopsis de Bary) as well as one species
(Phytophthora infestans (Montagne) de Bary).
A few key landmarks highlighted de Bary’s research
achievements. Firstly, in 1877 he published a nearly
700-page book titled, Vergleichende Anatomie der
Vegetationsorgane der Phanerogamen und Farne
(English translation: Comparative anatomy of the vegetative
organs of the phanerogams and ferns) that also included 241
woodcuts (de Bary 1877). This monumental study was
translated by British botanists Frederick Orpen Bower,
fellow of the Royal Academy who was awarded the
gold medal of the Linnean Society and the Darwin
Medal of the Royal Society, and Dukinfield Henry
Scott, former president of the Linnean Society, a member of
the Royal Swedish Academy of Sciences, who was also
Fig. 1 Professor Heinrich Anton de Bary (originally in Sparrow (1978))
awarded the Darwin Medal of the Royal Society. Secondly,
in 1866, de Bary published a ~300-page book titled,
In 1867, de Bary and his wife Antonie de Bary (previously Morphologie und Physiologie der Pilze, Flechten und
Antonie Einert) moved to Halle (Germany) to work at the Myxomyceten (English translation: Morphology and physiol-
University (currently, The Martin Luther University of ogy of fungi, lichens and myxomycetes; de Bary 1866), which
Halle-Wittenberg), and subsequently replaced Diederich he rewrote in 1884. Thirdly, de Bary’s most important and
Franz Leonhard von Schlechtendal, the German botanist innovative ideas resulted from his own ideas, namely, his def-
who co-founded Botanische Zeitung, a botany-centered aca- inition of symbiosis: Ba phenomenon in which dissimilar or-
demic research journal. Fittingly, de Bary later became a co- ganisms live together^ (de Bary 1879a, b; Ahmadjian and
editor and then editor-in-chief of Botanische Zeitung (Sparrow Paracer 1986).
1978; Horsfall and Wilhelm 1982). After leaving University In 1878, Professor de Bary was given the honor of an
of Halle, de Bary moved to the University of Strasbourg invitation to address the Association of German Naturalists
(France) to continue his studies, which were, in fact, viewed and Physicians (de Bary 1879a, b). It was here, describing
as his most productive years (Sparrow 1978; Horsfall and the intimate partnerships between algae or cyanobacteria
Wilhelm 1982). Over the course of 33 years as a professor (or both) and filamentous fungi, that Heinrich Anton
(1855 to 1888), de Bary trained more than 100 students who de Bary introduced the term ‘symbiosis’ in a biological
came from all corners of the globe to study in his laboratory context. It is worthy to note that German botanist Albert
(Fig. 2). In fact, de Bary viewed mentoring students to be one Bernhard Frank used the word ‘symbiotismus’ in a 1877
of his most important responsibilities, and persistently encour- manuscript and this may have stimulated de Bary.
aged them to be self-reliant, to think critically, and to over- Furthermore, the term ‘symbiosis’ was incorporated into
come difficulties and errors. Many of his students went on to human linguistics in 1622; thus, de Bary’s innovation
become distinguished scientists and educators (Ahmadjian was biologically centered (Richardson 1999). In 1879,
and Paracer 1986). de Bary’s speech was privately published in Strasburg,
Aside from mentoring students, de Bary authored more Germany, by the Verlag von Karl J. Trübner publishing com-
than 100 publications on fungi and plant diseases: those on pany as Die Erscheinung der Symbiose (de Bary 1879a). This
the parasitic oomycete, Phytophthora infestans, that infects seminal paper was translated into French (titled, De la
potatoes, the fungal pathogen of wheat and other grains, symbiose) and published in Vue Internationale des Sciences
Puccinia graminis, as well as studies of lichens. On 19 (English translation: International Journal of Science)
January 1888, de Bary passed away in Strasbourg, France, at (de Bary 1879b), but only fragments have been translat-
the age 57 of cancer of the mouth (Balfour 1889; Horsfall and ed into English (e.g., Ahmadjian and Paracer 1986;
Wilhelm 1982), and at the time of his death was one of the Sapp 1994). We hope that by providing a full transla-
most influential biologists in Europe (Sparrow 1978; Horsfall tion, researchers at all levels as well as historians of science
and Wilhelm 1982; Ahmadjian and Paracer 1986). will gain a greater understanding of symbiosis and the
Over the course of a career lasting nearly 40 years, de Bary origins of a discipline that investigates such a wide
was very productive, not only writing more than 100 range of associations.

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English translation of de Bary's 1978 speech, Die Erscheinung der Symbiose 133

Fig. 2 Professor Heinrich Anton

de Bary and members of his
laboratory in Strasbourg, France

2 Translation marks that I was supposed to have said, but that was not
in the lecture and that never could have been included. I
Die Erscheinung der Symbiose (‘de la Symbiose’) feel that I owe the reader who has become interested in
[The phenomenon of symbiosis] the subject matter, but is not familiar with relevant liter-
Lecture ature, a printed version of the subject matter as it is.
Held at the meeting of the German Natural Scientists I do not believe that any further arguments with the
and Physicians in Cassel A.W. correspondent are necessary. For readers who are
By A. de Bary not familiar with the subject matter, I have added foot
Professor of Botany at the University of Strasbourg notes with factual explanations.1
Strassburg, November, 1878.
Preface A. de Bary
The talk that is being published here was held at a gen-
eral meeting of the Cassel Natural Scientists. It was When I was trying to find a subject for this conference, I
intended for the named group of listeners, i.e. for natural was studying two plants that live in a special relationship. This
scientists and physicians, in order to give them a com- gave me the idea to talk about observations regarding dissim-
pact summary of a large number of connected natural ilarly named organisms that live together, in symbiosis, as we
phenomena and general aspects for assessing these. can call these associations. The present preoccupation with the
With the customary copy in the daily paper of the meet- subject, but also the consideration that similar relationships
ing, I believed that the talk had been adequately record- have become well known in the course of the past 10 years,
ed for the audience and for others for whom it might be are factors in deeming them to be of general interest. Thus, this
of interest. I felt that an additional publication would be talk will be a consideration of such symbioses, namely, the
superfluous. And even now, in spite of having been living together of differently named organisms. I have decided
requested to make the lecture available to a larger pub- to bear with this subject, in spite of the fact that the topics at
lic, I would have declined if it had not been for a sup- our meetings should deal with contemporary issues, critique
plement of the Augsburger Allgemeiner Zeitung and history of methods used in science and teaching. The
[Augsburg General Newspaper] no. 296, October 23, presentation of current research results will certainly also be
1878, in which a critique by A.W. was published. Or of general interest.
perhaps I should rather call it a provocation. The re-
marks of the A.W. correspondent were not suited to give
the reader an accurate impression of what the lecture 1
We have not translated the numerous footnotes that are in the German
intended to convey. It even contained a text in quotation but not in the French version, since they were not part of the original talk.

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134 N. Oulhen et al.

I am going to talk mostly about observations made in the plant left-overs of the food that the larger has attained for itself.
kingdom; first, because the nature of these associations are easier They are the commensals of van Beneden.
to observe, and also because the corresponding phenomena It’s clear that similarities exist between all of these relation-
found in the animal kingdom are already known to people pres- ships and strict parasitism; there are also intermediate degrees.
ent here, or can be read about in the popular book written by In the plant kingdom, the last two categories are less com-
[Pierre-Joseph] van Beneden: Animal parasites and messmates. mon. However, a careful study found mechanisms that are
I will not have time to talk much about this subject in the close to the mutualism of van Beneden with epiphytes that
limited time that I have here, so I will simply indicate the main are very well represented in the tropical world by hundreds
points, and explain them with good examples. of orchids and aroids. These plants attach to the bark of the
The most well-known and most exquisite example of sym- tree and use the products resulting from the exfoliation of the
biosis is holoparasitism, the state in which an animal or a plant bark. We find these interactions everywhere in this country,
is born, lives, and dies on or in an organism that belongs to a like the moss growing on bark – not to mention the smaller
different species. This organism becomes the home of the species – plants that choose to live in the desquamination of
parasite and provides the parasite with its entire nourishment. the bark, some having no preference for a specific tree species,
In one word, it is its host, and since the parasite attains its others preferring one species.
nourishment either from the body of the host or from the food All plants with chlorophyll are highly independent of their
it consumes, it lives off the organism. The relationships be- host concerning their nutritional processes. We could at most
tween the parasite and its host are, as we know, very diverse, consider these epiphytic organisms as commensals of their
particularly regarding the dependency of one on the other. plant hosts; but this term could be applied to all non-
Some parasites are completely dependent on different hosts parasitic plants growing in the same location, to the extent that
that may vary according to their developmental stages. That is they share carbon dioxide, water, and nutritive substances
the case of the Cestoda (tape worms), or the rust fungi on from the ground. Using van Beneden’s strict definition of
Berberis, the Boraginaceae, and the Poaceae. On the other commensalism, it cannot exist in the plant kingdom.
hand, some parasites can live with very different hosts, but can This is enough to demonstrate that there are not strict par-
also, at specific times of their life, live without hosts. This is allels between phenomena observed in the two kingdoms.
the case for several blood sucking insects, for some fungi, and There are, moreover, among the plants, additional associations
several parasitic insects. The muscardine fungus (Botrytis between differently named species that cannot be classified in
bassii), for example, does not spare any species of insects the categories previously mentioned. The association between
when it meets them at the right moment. However, it can also Azolla and Anabaena as mentioned at the beginning of this
grow freely, without a host, and produces spores that will talk is such an example.
reach new victims. Intermediate relationships exist between Azolla is the name of a genus of fernlike plants that look like
these two extreme cases. large, foliated mosses and that grow on the surface of water as
Another point to consider regarding the relationships be- the duckweeds (Lemnaceae) do. The stem is very branched
tween parasites and their hosts is the negative effect that the first and linked to abundant roots, and has two rows of leaves that
has on the second during development. Antagonism, a fight, are closely spaced and oriented horizontally on the water sur-
must occur between the two, depending on the nourishment face. Each leaf is composed of two lobes, superimposed and
uptake of the parasite. The course and the outcome of this fight spread at the surface of the water. Despite an exceptional pe-
can differ greatly. Sometimes the parasites barely affect the culiarity, the structure of this plant is not essentially different
hosts, in several fish for example. On the other hand, disease from other plants that have a similar lifestyle. On the lower
and death can be caused immediately by the parasite, as is the surface (oriented towards the water) in the upper foliar lobe,
case of humans infected by Trichinosis, or in potatoes infected there is a small opening leading to a relatively spacious cavity,
by Phytophthora. However, different relationships exist be- which is covered by special hairs. In this cavity, lives a blue-
tween other organisms. They are similar to parasitism and are green algae composed of a single row of cylindrical cells,
often classified in this category, but they are essentially different. elongated and embedded in a gelatinous sheath, as is charac-
Many smaller animals live on larger animals and feed on teristic for several groups of Nostocaceae and especially for
their waste: epidermis that is exfoliating, feathers, hairs, etc. Anabaena. When the leaves die, the Anabaena within also
This is the case for several species of Trichodectes and dies, according to what we have been able to observe. There
Philopteri; they can feed from the skin mucus of the fish, like are no other algae in this cavity. How does this unusual visitor,
the Arguli. These are van Beneden’s mutualists; they are in a without exception, enter each leaf and where does it come
relationship of mutual enhancement with their hosts. By living from? It cannot be found outside of the plant, on the leaves
off the waste of their hosts, they take care of its hygiene. of the adult, or even at the entrance of the cavity. It is only
Other small animals live in or near larger animals, to feed found in one other location: a little bit below the extremity of
from the crumbs that fall from the table of the rich, from the the branch, that still grows in length, as in other plants of the

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English translation of de Bary's 1978 speech, Die Erscheinung der Symbiose 135

same family, and produces new leaves and new branches. This There is one form of vegetation, an extensive group, com-
extremity is curved and shaped like a hook oriented upward. A posed of thousands of species that is an association of two or
concave space is located just below it and surrounded by the three different species that also can only exist through this
structures that will give rise to the leaves and the branches. association. I am talking about organisms known as the li-
This concave space is also inhabited by Anabaena. It is located chens. Among them, you probably know the reindeer lichen
just below the extremity of the young developing branch, and and the Iceland moss. Everyone has also seen how, especially
Anabaena immediately locates to the indicated place. The in the mountains, they may abundantly cover the surfaces of
young leaves are in contact with the algae; the upper lobe is rocks, peat, and the trunks of the trees.
flat at the beginning, but then a bulge in the shape of an annular Most of us learned at school that lichens are cryptogams
bead grows quickly and forms the cavity with its opening. As and their method of fructification is exactly that of the asco-
soon as this bulge starts to form, a part of the algae gets trapped mycete fungi. Their structures are also very similar, except
in the center, and grows within the cavity. As the stem extends, that they always contain cells with chlorophyll that fungi do
this foliar part containing Anabaena becomes isolated from its not have. Because of this specificity, lichens can assimilate
first location. I have already told you that this interaction was carbon dioxide, explaining their ability to live on naked rocks
first described by [Georg] Mettenius and [Eduard] Strasburger or other substrates deprived of organic compounds. Fungi
and that they found no leaf without a cavity, and no cavity deprived of chlorophyll require organic compounds.
without Anabaena. The following part is no less interesting. The masses of green cells that characterize the lichens had
We know four species of Azolla that are quite similar, but the most unusual fate in the history of science, until it was
clearly delineated by differences in their fructification. Two demonstrated 10 years ago that they are not really part of the
of these species are very common in America and Australia; plant, which has the same vegetative and fruiting body as the
the third one is in Australia, Asia, and Africa; the fourth one is, fungus. They are algae that live and grow in association with
as far as we know, limited to the area of the Nile [River]. In all fungi that cannot exist without this singular association. A
these species, and in all the samples that were studied, we specific species of fungus and a specific species of algae create
found this association with Anabaena as described, and totally in a unique association a specific lichen; without this associa-
identical in all the details. Thus, it is not possible, so far, to tion, the lichen would not exist. If the spores of the lichen,
distinguish the species of Anabaena according to the Azolla in which are produced abundantly, are sowed under favorable
which they were found. conditions, only small fungi grow and quickly die. The fungi
There are a number of cases in which species closely relat- can only develop to lichens if they associate with the correct
ed to the Azolla-Anabaena, commonly described as Nostoc, alga. Each species of lichen fungus only associates with a few
live in terrestrial plants, also in cavities, but with always less species or with only one species of alga; among these fungi,
regularity than the described example. They can be absent, or many related species can form these associations.
can come from outside during the later stages of development. However, the number of algae is lower than the number of
I only want to refer, as an example, to the roots of the cycads. fungi that can produce lichens, and lower than the number of
This plant grows slowly and when relatively young begins to the corresponding lichens; because according to [Agustín]
develop a thick tap root that becomes branched in and on the Stahl’s reports, it is clear that one single species of alga can
ground, as other roots do. At the base of the root – I do not be used by several or perhaps many fungal species to form
know if this is always the case – one or two pairs of root many lichen species. I will have to come back to this subject to
branches develop. Generally or maybe always, they grow per- discuss the forms of the association and the relationships be-
pendicularly upwards, branch, change directions once or tween the associated species.
twice, and form spadiceous bulges at their extremities. When we observe more closely the phenomena described
Similarly, dichotomously branched roots appear later, often above, we find in the azollas and the cycads as well as in
in abundance and very close to each other, on the branches lichens, intimate associations of different species, but never
of the tap root and spread on the ground. Frequently, but not an organization that fits one of the categories described at the
always, Nostoc can enter between the cells of the dichoto- beginning of this study. For the reasons that I have already
mously branched roots; this is followed by specific changes explained, we cannot strictly speak of commensalism or
in the structure of the root branch. Under the bark, a paren- parasitism.
chymal layer develops that barely differs from the roots in The Anabaena of Azolla, and the Nostoc of the Cycas’s
absence of Nostoc. Soon, this layer becomes an arched struc- roots live in specific locations, but they do not live at the
ture, held by thin strands between which are located large expense of their hosts; there is not even evidence that they
spaces. The strands are elongated cells of the parenchymal take advantage of them. The Nostoc of Cycas can thrive ex-
layer. The spaces are filled with abundantly growing algae. cellently in water, even without having this hostel. When we
This is, again, a specific association; we know a number of artificially isolated it, the Anabaena of the Azolla also seemed
others, but they are not as remarkable. to live in water without a living host, which has not yet been

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136 N. Oulhen et al.

verified. We can theoretically assume this a priori for and lichenism are special cases in this establishment of asso-
Anabaena as well as for the Nostoc-form. Not only because ciations in which the term symbiosis serves as a general de-
they have the same structure as plants with chlorophyll that scription. Do we want to differentiate the main categories? We
can live without organic compounds, but also because we suggest two categories: the antagonist symbiosis in which the
know many structures that look exactly like them, which partners combat one and other, and the mutualistic symbiosis
means that there are many Nostoc and Anabena species that in which there is a reciprocal benefit for the symbionts, but
do not grow in living accommodations, but vegetate freely in here, again, we cannot define exact boundaries.
water or on the ground. The boundaries are not well defined if we want to distin-
The term mutualism would be best suited to define the life guish associations of symbionts that are strictly united for their
of the Nostoc that we have just talked about, if we accept that common benefit in contrast to those that we can group under
the host and the parasite are useful for one and other, i.e. do the term of sociability. Examples of the latter are very diverse.
each other a few favors. It is, however, doubtful that there are A Mexican bird, the cowbird, lands on the nose of a bison
mutual advantages to the partners. We can definitely say that stuck in the mud and is on the outlook for mosquitoes that
they do not harm each other significantly, because, if this were want to crawl into the animal’s nose. Another example: On the
the case, the association would not exist. It is likely that the mountain, Serra dos Orgaos, in Brazil, an aquatic plant,
host protects the little algae in different ways. But presently, Utricularia nelumbifolia, which is probably insectivorous,
we have no evidence of the mutual benefits that they could lives on the arid rock slopes, a phanerogam with chlorophyll.
afford each other. It only grows in water, locked in the funnel-shaped center of
The usefulness of the relationships for the lichen partners the leaf rosettes of a member of the Bromeliaceae, common in
varies, but also differs from that of the relationships observed these regions. It produces stolons, almost like those of straw-
in animals. Without making any huge mistakes, but only for berries that form a new plant when they reach another rosette.
very few of them, can we talk about real parasitism. This is New flowers and stolons form on this new plant. These asso-
because the fungus creates its home in or on the algae, the ciations are similar to the ones we have referred to as symbi-
smaller partner, and lives at its expense. But even in the best osis, but we can only use this term if we also use it for all the
scenario, the term parasitism is not strictly accurate. For most other relationships such as the ones that exist between the
of the lichens, the relationship is quite different. The algae can insects that enter the flowers and the flowers that re-
usually live alone. We can not only artificially isolate it and ceive the pollen from the insects, or between animals
observe its independent growth and reproduction, but we also that look for food or for a shelter and the other animals or
often see the lichen algae in nature without its being part of a plants that provide them. I have no objection to this general-
lichen. This is not the case for the fungus of the lichen. It ization, as I have tried to demonstrate the similarities between
cannot develop by itself, as already mentioned, and dies these associations.
quickly if it does not find an alga. To grow and develop, the With the proof of the similarities of these associations, the
fungus needs the alga’s carbon dioxide assimilates. However, exceptional position occupied by certain parasites disappears,
it does not simply stay in or on the algae, it encloses it with its even though it may seem special among the close relatives.
body, growing so extensively that for most of the lichens, it We also reject the old opinions that they were borne from the
forms most of the overall mass. The alga only represents a juices or rotten tissues of the host. And, similarly, the lichens
small part, one tenth, or maybe less. According to this volume, also lose their position that at first glance seemed so
the fungus would be the host, and the algae would be the exceptional.
tenant. But the host depends on the tenant to survive – it is 2
The lichenologists became extremely upset upon hearing
what usually happens in real life. The tenant is given the best of this algal-fungal interaction, feeling that their darlings were
of care; not only is its growth not inhibited, but is even better being degraded, convinced that it was unbelievable that li-
than when growing alone; its growth is coordinated with that chens were not independent organisms, but rather – in their
of the host. Finally, by penetrating deeply into the hard rock, opinion – an illegal association between a fungus and an alga.
the host is in charge of attaching the body to the substratum, The outrage ought to disappear, considering the fact that there
but also for providing necessary components of volcanic ash is nothing illegal going on, but rather that these are special
to the joint household. cases that occur everywhere in nature with a thousand differ-
We cannot continue to discuss the extremely interesting ent forms. We can only thank Schwenderer for clarifying the
detail regarding lichen structure and economy, but must limit previously puzzling structure of lichens as such a unique form
the discussion to that which has already been said, adding that of symbiosis.
there are many diverse phenomena regarding the living to-
gether of organisms of different species that are associated
with parasitism, mutualism, etc. They are too diverse and 2
The following text, the end of which will be marked by another foot-
complex to be put into categories. Parasitism, mutualism, note, was only in the German, but not in the French translation.

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English translation of de Bary's 1978 speech, Die Erscheinung der Symbiose 137

The proof that the examples discussed belong to the large Of all the environmental factors, the effects of dissimilarly
number of interactions between different organisms is not in named organisms on one and other are particularly outstand-
itself an explanation for the interactions, assuming that this is ing and are strong reciprocal determinants of morphology and
understood as one example of an empirical rule that had pre- behavior. The morphology and features of both the flowers
viously been seen as one isolated case. A real explanation can that bees frequent and that of their visitors, the relationship of
be gained if regarded from the same standpoint and within the the azollas with their anabenas, and a thousand similar rela-
same limitations as for other such phenomena of the same tionships can only be understood as a result of mutual adap-
category. And conversely, they may contribute to understand- tations. These cases can also be inherited, predetermined
ing the entirety. states. There are many other examples which confirm our
The first of these assumptions is obvious, and it goes with- expectations that symbioses are determinants of morphology.
out saying that regarding the explanatory aspects, the theory It would take far too much time to remove the azollas from
of evolution as developed by Darwin is meant. Only this the- the cavities of Anabena, aside from the fact that it would not
ory, which includes the principles of breeding, is able to pro- make any sense. There would be the insurmountable difficulty
vide a scientific explanation for the phenomena that we have that removal of the little guest would undoubtedly injure the
discussed. Any further discussion of this point would be su- delicate structures of the host. However, there are not any
perfluous. And, I do not need to mention the limits that the better examples.
explanation temporarily has regarding the attributes of orga- Many strict parasites influence the morphology of their
nized substance and the prevailing lack of knowledge of the hosts. Wolf’s milk (Euphorbia esula) completely changes its
physiological fundaments known under the collective name of morphology following intrusion of a parasitic fungus that to-
adaptations of normally combined processes. Within these tally transforms the form of the summer shoots. A similar
limits, on the basis of the theories of evolution and breeding, freeloader fungus (Aecidium elatinum) intrudes into the buds
we can understand the habits of the cowbird and of insects that of the European silver fir (Abies pectinata) [Abies alba]. The
visit flowers, the relationship between Azolla and Anabena, uninfected branches have horizontal, bilateral branching and
the interactions of the lichens and of parasites, but also the evergreen leaves. The branches occupied by the intruder grow
peculiarities of morphology and structure that originated his- upright with whorled ramifications, losing their leaves every
torically from successively inherited phenomena. year and developing new ones every spring, developing little
If these phenomena can be subordinated to the theory of fir trees on the intact branches that can become 10 or more
evolution, then they are evidence for the theory and contribute years old.
to its totality. A closer examination of symbioses shows that a The parasites are directly responsible for these changes
more important contribution can be found elsewhere. We have in morphology. They do not occur when the parasites are
ample reason to agree with Darwin to say that successive absent. They can be intentionally induced and prevented.
adaptations and the correlating changes of morphology and Perhaps these examples should be disregarded since they bor-
transformations of organisms occur, and must occur, as a con- der on pathogenicity; and since they have similarities to the
sequence of the influence of the environment on the organisms formation of galls and tumors, their exemplary status is weak-
and on their capacity for transformation. Through the interac- ened – but admittedly not more than that. Where does the
tions of these two main factors, we can explain the forms and border between pathological and non-pathological transfor-
mechanisms that presently exist. mation differ more than a conventional differentiation?
Most of these morphologies and mechanisms are fully de- We’ll refrain from further consideration of such examples,
veloped and inherited traits; the transformations through because this is not necessary.3
which they originated did not occur before our eyes and we As mentioned earlier, when Nostoc enters the dichotomous
are not in the position to make them arbitrarily appear and roots of the cycads, the structure of these roots changes con-
disappear. Their origin lies in prehistoric times, a period which siderably. Large spaces appear in the compact parenchyma of
can be only more or less accurately determined. Regarding the roots to house the visitor; they are formed by a specific
the azollas, for example, the development of the cavity in orientation of the growing tissue and do not appear in the roots
which Anabena resides arose before the spatial separation in absence of the visitor. We saw something similar, but more
and thus differentiation of the four present-day species. obvious, with the algae and the fungi that produce the lichens.
We attain information regarding the processes involved We have already talked about the features of the fungi. The
in development of the present conditions from our expe- alga is considerably modified when it unites with its compan-
riences with variability, the capacity for transformation of ion. The orientation of growth that influences the shape is
species, from results of intentional breeding, in part modified. A gelatinous stem that Nostoc, the algae of
through comparison of parallel existing morphologies,
from predetermined inherited morphologies and from 3
This is the end of the text that is present in the German, but not in the
embryonic developmental states. French, text.

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138 N. Oulhen et al.

gelatinous lichens, produces is flat or slightly spherically has greatly expanded. Over the following ~130 years (i.e.,
shaped, branching regularly into a fructicose body. The chlo- until the present), our comprehensive knowledge of symbio-
rophyll cells, round or elongated, found in Pleurococcus and ses stems from various systems, including: (1) the bobtail
Stichococcus, change their shapes as soon as the lichen- squid Euprymna scolopes and its bioluminescent bacteria
fungus captures them. The orientation of their divisions can Vibrio fischeri (Nyholm and McFall-Ngai 2004); (2) hard
gradually change, but are variable depending on the fungus corals and zooxanthellae (Muller-Parker and D’Elia 1997);
with which it associates. (3) the gutless deep-sea tubeworm Riftia pachyptila and
In these plants, and in the case of Cycad, pathological sulfur-oxidizing bacteria (Cavanaugh et al. 1981); (4) isoptera
changes do not occur, not only because we do not have con- (termites) and their microbiome (Warnecke et al. 2007); (5)
ventions to agree on what is healthy and what diseased, but Leguminaceae and root-based nitrogen-fixing bacteria
also because there is no evidence of a decrease in vital energy, (Franche et al. 2009); (6) lichens (Nash 2008); and (7) mycor-
of faster death, nor any evidence of a sickly state. Instead, the rhiza (Harley and Smith 1983); numerous other examples of
reports written by Stahl have demonstrated that right after symbiotic interactions are discussed by Egerton (2015).
their association with the fungus of the lichen, the cells of A common characteristic of these symbioses is that symbi-
the algae become much larger, contain more chlorophyll, are onts associate with a specific species of bacterium or (more
stronger in every way. Beyond doubt, according to data that accurately) a community of bacteria and other microbes
have been known for a long time regarding the structure of the (fungi, viruses, bacteria, and archaea). Moreover, each
lichen, all of these characteristics are retained for the entire life partner provides a nutritional and/or metabolic advantage
of the lichen, sometimes for several dozen years. to the other, which might be termed altruism. For example,
Here, and in many more examples that I could have men- most aphids (plant lice) harbor intracellular bacteria of the
tioned, we can see changes in morphology that we cannot genus Buchnera, where the primary role of the bacteria as a
explain as pathological in the mutual relationships between vector for nitrogen recycling is to provide amino acids to the
symbionts with dissimilar names. The researcher can arbitrari- host, while the host supplies the symbiont with nutrients via
ly make these changes appear or disappear by uniting or sep- phloem sap, vertebrate blood, or wood (Douglas 1998).
arating the symbionts. But, because the phenomena that we In recent years, the field of symbiosis has focused on
have described as symbiosis are only specific cases among the understanding partnerships between the host and its
many relationships that exist between organisms, these are microbiome: the collection of bacteria, fungi, viruses,
merely a contribution to understanding the entirety of associ- and archaea intimately associated and specific to the
ations between organisms. By themselves, these phenomena host. Mediating this revolution are advances in sequenc-
may not seem to be important, and for some people it might ing platforms (i.e., next generation sequencing) and cor-
have appeared unnecessary to pay attention to them; they are responding bioinformatics techniques (i.e., metagenomics)
however of great value because they are experimentally (Jumpstart Consortium Human Microbiome Project Data
accessible. Generation Working Group 2012; Shokralla et al. 2012). In
The theory of evolution has often been criticized for its lack brief, studies using these techniques show that bacterial sym-
of experiments; this charge is wrong, because, as has often bionts are critical, if not essential, players in development,
been emphasized, we can find important reports that support immunity, regeneration, and disease resistance (McFall-Ngai
this theory in the breeding of animals and plants. Independently et al. 2013; Bordenstein and Theis 2015; Gilbert et al. 2015;
of the importance that we give to natural selection, which re- and references therein). A synthesis of host-microbe studies
sults in gradual changes of the species, it is desirable to see the led to proposing the holobiont or hologenome theory of evo-
opening of a new field for experiments. That is why I wanted to lution, which states that the collection of host and symbiotic
bring your attention to these experiments, even if only to clarify microbes is a unit of selection and a product of co-evolution
some of the observations. I have not talked about any new (Margulis 1991; Zilber-Rosenberg and Rosenberg 2008;
observations. All the examples that I have mentioned are well Rosenberg et al. 2009; Bordenstein and Theis 2015).
known. Evidences to support the fundamental theory that we The term ‘symbiosis’ first applied to biology in 1878 by de
have talked about are found everywhere. We just have to care- Bary is now accepted without question by the life sciences,
fully look around. and these intricate partnerships are thought to be a major driv-
ing force in evolutionary biology, as hosts and their symbiotic
microbiota acclimate on short timescales and potentially adapt
3 Concluding remarks over long-term timescales. The recognition that dissimilar or-
ganisms can live harmoniously in close association with one
Since Heinrich Anton de Bary’s address to the Association of another has had a more significant impact than de Bary could
German Naturalists and Physicians in 1878, the recognition have realized, and the extent to which this is the case is likely
and appreciation for symbiotic partnerships and associations beyond the scope of our present understanding. By publishing

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English translation of de Bary's 1978 speech, Die Erscheinung der Symbiose 139

de Bary’s 1878 speech in English, we hope this scientific Egerton FN (2015) History of ecological sciences, part 52: Symbiosis
studies. Bull Ecol Soc Am 96:80–139
landmark will be more widely recognized for its significance,
Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria
its forward thinking, and as the origin of all studies on associated with leguminous and non-leguminous plants. Plant Soil
symbioses. 321:35–59
Gilbert SF, Bosch TCG, Ledón-Rettig C (2015) Eco-Evo-Devo: devel-
Acknowledgments We thank Brown University and the University of opmental symbiosis and developmental plasticity as evolutionary
North Carolina at Charlotte for financial support, Dr. William Martin agents. Nat Rev Genet 16:611–622
(University of Düsseldorf, Germany) for obtaining a difficult-to-get orig- Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic Press, Inc
inal French version of de Bary’s speech, and Dr. David Richardson (Saint Horsfall JG, Wilhelm S (1982) Heinrich Anton De Bary: Nach
Mary’s University, Canada) for providing critical comments on an earlier Einhundertfünfzig Jahren. Ann Rev Phytopathol 20:27–32
draft of this manuscript. Jumpstart Consortium Human Microbiome Project Data Generation
Working Group (2012) Evaluation of 16S rDNA-based community
Compliance with ethical standards profiling for human microbiome research. PLoS One 7:e39315
Margulis L (1991) Symbiogenesis and Symbionticism. In: Margulis L,
Conflict of interest The authors declare that they have no conflict of Fester R (eds) Symbiosis as a Source of Evolutionary Innovation:
interest. Speciation and Morphogenesis. Massachusetts Institute of
Technology, Boston, pp. 1–14
McFall-Ngai MJ, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo
T, Douglas AE, Dubilier N, et al. (2013) Animals in a bacterial
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