Ramon Margalef López (1919-2004) was a pioneer who made outstanding scientific contributions in limnology, oceanography and ecology. He was an exceptional scientist, teacher and mentor and is considered one of the founding fathers of modern ecological theory. However, he often qualified himself as a naturalist and grounded his thinking on long hours of painstaking observation of nature accompanied by field work and imaginative experiments. Much of this activity was carried out in Barcelona, at the Instituto de Investigaciones Pesqueras (Institute of Fisheries Research, IIP) of the Consejo Superior de Investigaciones Científicas (Spanish National Research Council, CSIC), now renamed Institut de Ciències del Mar (Institute of Marine Sciences, ICM). As part of the celebration of the 100th anniversary of Margalef’s birth, this article aims to give an overview of his contributions to the journal Investigación Pesquera and to its successor, Scientia Marina.

This section will provide only a brief account of the unusual career path of Ramon Margalef. More detailed explanations of his biography and thinking can be found in publications such as Bonnín (1994), Durfort (2005), Peters (2010) and in numerous interviews and press articles.

From a very young age, Margalef was an enthusiastic observer of nature, in particular of aquatic organisms, and as a teenager he continued with his self-taught naturalist studies. In 1938, two years after the Spanish Civil War broke out, Margalef was conscripted into the Republican Army. After the end of the war, he was drafted again, this time to serve on the winning Nationalist side until 1943. Margalef persisted with his scientific observations and his merits were recognized by influential scientists and naturalists in Catalonia, who encouraged him to study Natural Sciences at the University of Barcelona, where he graduated in 1949. In the same year the CSIC created the Marine Biology Section of the Instituto de Biología Aplicada (Institute of Applied Biology, IBA), which in 1951 became the IIP, under the direction of Francisco García del Cid. Margalef, who had obtained his doctoral degree in 1951, joined the IIP as a researcher in 1952. After the sudden death of García del Cid in 1965, Margalef became director of the IIP and served in this position until 1967, when he occupied the first Ecology chair in Spain at the University of Barcelona. He retained a part-time position at the IIP until he was forced to give it up in 1977. He retired officially in 1993, but continued his scientific work until the last years of his life. He died in 2004, having authored several books and nearly 600 publications, 87% of which are single-authored, and in only 3.9% he is not the first author (Peters 2010).

Margalef’s initial work as a naturalist dealt mainly with observation of organisms of continental waters, a passion that he kept throughout his life. After his engagement at the IBA, he started studying the marine ecosystem. As he wrote in an unpublished autobiography (Margalef 2004):

“La vida aquàtica apareix dividida en... dos reialmes i aquesta situació resulta força interessant per aprendre aspectes de la interacció entre el medi intern i l’entorn de la vida... una cama o peu en cadascun dels grans sistemes aquàtics del planeta... enriquia qualsevol estudi comparat”. (“Aquatic life is divided into... two realms and this situation is quite interesting to learn aspects of the interaction between the internal environment and the environment of life... a leg or foot on each of the great aquatic systems on the planet... would enrich any comparative study”).

Both as a limnologist and as an oceanographer, Margalef’s observations built the taxonomic basis for the scientific study of planktonic organisms in Spain. However, in parallel with this descriptive effort, Margalef strived to deepen his understanding of the relationships between hydrographic factors and plankton ecophysiology and to find general principles underlying phytoplankton diversity and succession. From the beginning of his scientific career and throughout his life, Margalef assembled a theoretical framework that made him one of the most influential ecologists of our times. Some of Margalef’s best known early theoretical contributions appeared in English in books (Margalef 1968 and Margalef 1997b) and international journals, but the fundamentals for many of them could be found in the publications of the IIP.

A number of Margalef’s early publications (between 1944 and 1958; Table 1), mostly on continental waters but also on marine phytoplankton, appeared in the journal of the IBA, Publicaciones del Instituto de Biología Aplicada, which was discontinued in 1973. After the appearance of Investigación Pesquera, in 1955, Margalef contributed 65 articles to this journal between then and 1972 (averaging more than three papers per year) and one in 1987 (Table 2). The Investigación Pesquera series also included several monographic issues dealing with meetings or seminars organized by Margalef: the Seminar on Mathematical Ecology (Margalef 1970a), the Working Conference on Analysis of Upwelling Systems (held in March 1970), whose papers were published in Investigación Pesquera 35(1), and the Seminar on Factor Analysis in Ecology and Taxonomy (Margalef 1972a). Margalef also contributed to Scientia Marina (in 1994, 1997 and 2001; Table 3), which replaced Investigación Pesquera in 1989 (see Lleonart and Olivar 2011 for a history of these journals) after the IIP became the ICM. As was required at the time, all articles by Margalef in Publicaciones del Instituto de Biología Aplicada and most in Investigación Pesquera were written in Spanish [exceptions were Margalef and Estrada (1971) and the last two, Margalef (1979), Margalef and Estrada (1987)]. Those in Scientia Marina were in English. In addition to his publications in Investigación Pesquera, Scientia Marina and many other Spanish and international journals (see Peters 2010 for a comprehensive list), Margalef also contributed to sister publications of Investigación Pesquera at the IIP, such as Resultados de Expediciones, Suplemento de Investigación Pesquera (from its beginning in 1972 until 1979, the title was Resultados de Expediciones Científicas del Buque Oceanográfico Cornide de Saavedra. Suplemento de Investigación Pesquera), for which he wrote six papers between 1972 and 1975, and the proceedings of the Productivity and Fisheries Meetings, a series of seminars organized by the IIP, which appeared in specific publications in 1954, 1955, 1957, 1960 and 1965.

The objective of this article is to present a brief overview of the published contribution of Margalef to Publicaciones del Instituto de Biología Aplicada, Investigación Pesquera and Scientia Marina. In order to do this, we propose a rough classification into four main aspects covered in these articles: Margalef as a naturalist; Margalef as a scientific illustrator; physical models and “rain-making” machines; and theoretical ecology. This arrangement should be considered only as an operative approximation, because, from the beginning of his career, one of the characteristics of Margalef’s scientific thinking was his integrative and multidisciplinary approach. In addition, he would often revisit and rework previously established concepts.

Science has always included a strong component of visual effort. Especially for natural history, which is largely based on observation, illustration is the perfect tool for studying, understanding, describing and communicating the characteristics of the structure, environment and life cycle of animals and plants and for helping to understand new concepts and abstract ideas about the functioning of nature.

Coinciding with the increasing interest in natural history in the late 18th century, the collaboration of naturalists with expert artists brought added value to their studies (Dance 1990). Of course, naturalists with artistic skills had a supplementary advantage, adding to their scientific background the capacity to reproduce, with the fidelity required by the most rigorous taxonomist, details that even the use of mechanically reproduced images could often not provide (Alcaraz et al. 2015). Ramon Margalef was one of these scientists, a passionate observer of nature in whom a vast biological knowledge coincided with unusual drawing skills.

Margalef was attracted from his childhood by the beauty of life-forms. He observed, collected, and drew the little organisms that thrived in the pool at the small garden in the back of his house and in patches of abandoned fields. This early fascination with nature was documented in a number of notebooks full of drawings and annotations about insects and small aquatic animals and plants (Peters 2010), the prelude to his crucial role in the foundation of studies on aquatic ecology in Spain.

For more than a decade, from 1943 to 1955, Margalef’s scientific publications were a miscellaneous representation of his interest in aquatic life in general. With the exception of a couple of studies on marine plankton, these publications formed part of a systematic and conscious approach to futhering knowledge of life in freshwater bodies. Most of the fundamentally descriptive papers on the morphology, habitat, life cycle and behaviour of a variety of aquatic organisms, from algae to insect larvae or crustaceans, are illustrated by wonderful original drawings. In his early papers dealing with freshwater fauna and flora (Fig. 4), the illustrations complementing the text were wonderful fine-line and stippling drawings reproducing species with minute morphologic details, artistically arranged in plates, some of them signed with his artistic cipher (Margalef 1943, 1944).

When Margalef joined the IBA in 1945, his studies on marine plankton took on new energy, although he wrote few papers on this topic within his abundant and varied scientific production from 1945 to 1955 (Table 1). Two examples of his scientific rigour and technical and artistic ability stand out from this period: the introduction to the study of marine plankton (Massutti and Margalef 1950) and a monograph on Iberian freshwater crustaceans (Margalef 1953c), both with excellent original illustrations that are still being used as valuable taxonomic guides.

When Investigación Pesquera was launched, most of Margalef’s scientific papers concerning marine life were published in this or in sister journals (although there are also unpublished excerpts from Reuniones sobre Productividad y Pesquerías, mimeo records of communications mainly on technological aspects), while his limnological studies were still being published in Publicaciones del Instituto de Biología Aplicada.

Around half of the publications of Ramon Margalef on marine plankton either in Publicaciones del Instituto de Biología Aplicada or Investigación Pesquera consist of studies about the community composition, spatial distribution, temporal succession and production of phytoplankton in coastal localities of the Mediterranean or the Atlantic. These publications, besides being an exhaustive inventory of species and environmental data, include original illustrations of particular species, fine-line drawings of great taxonomic fidelity that are arranged in plates of unusual aesthetic taste (Fig. 5).

Aside from the naturalistic traits, Margalef’s new ideas required texts and verbal descriptions to be complemented with illustrations capable of going beyond the limits of language. Graphs, charts and diagrams were used to facilitate the communication of abstract concepts by means of formal similitudes aiming to concentrate huge amounts of information into a form in which it would be more easily absorbed by the reader (Tufte 1983). As the early papers published by Margalef in Investigación Pesquera were devoted to the description of seasonal cycles of phytoplankton, the interaction regularities observed between environmental variables and quantitative plankton data had to be synthesized in charts and infographic solutions that helped explain novel concepts and theories, defined as Margalef’s “drawn ideas” (Segarra 2019).

The use of infographics covers many of Margalef’s studies, ranging from the relations between temperature and morphological and physiological characters such as size, metabolic activity and water content in phytoplankton cells (Margalef 1953b) to the composition of autotrophic pigments in phytoplankton and other organisms in relation to community structure (Margalef 1964b). His models on the formation of plankton patches, including the particular case of noxious phytoplankton blooms (spatial distribution, abundance and even demographic composition) as a function of diffusion rate, motility, reproduction and mortality (Fig. 6), were among the first contributions in which the use of infographics helped the understanding of complex physical and biological interactions (Margalef 1956e, 1957c).

The new style of graphic representations also helped to explain the complex, multidimensional relations between hydrography and fisheries (Margalef and Andreu 1958), to describe the patterns in the spatio-temporal variability of phytoplankton groups as defined by their life-style (phytoplankton life-forms) according to the effects of a number of variables, and to express the relation between structural properties and function (Fig. 7) (Herrera and Margalef 1957, Margalef 1957e, 1961b, 1963c, 1970b, Margalef et al. 1959, Margalef and Herrera 1963). Probably the most widespread and best known of Margalef’s “drawn ideas” is the simple graphic presentation of the temporal succession of phytoplankton life-forms as selected by the possible combinations of mechanical energy (turbulence) and nutrients, universally known as Margalef’s mandala (Margalef 1978).

Those who worked closely with Margalef would have seen and frequently used (and sometimes suffered) apparatus that could not be precisely classified as standard oceanographic equipment. His students had a term to define these inventions: Margalef’s “rain-making machines”. In Spain, a broken country after the civil war, sampling, measuring and experimental devices and scientific equipment in general were simply non-existent or impossible to acquire. Therefore, Margalef conceived, designed and sometimes built himself the required equipment, as happened with his first microscope, made by joining optical pieces found in flea markets to a self-made mechanical stand, with a camera lucida he also made and adapted to it (Fig. 8). Other miscellaneous inventions include laboratory columns with electrodes to study the suspension of phytoplankton according to changes in their physiological state, such as those produced by photosynthetic activity that could modify their surface electric charges (Margalef 1957b), an idea that was further developed into a device for measuring depth differences in electric potential in the marine water column, as a proxy for vertical water movements, phytoplankton abundance and vertical migration, or photosynthetic state (Margalef 1967b). Most of the prototypes of new apparatus were made with Meccano, a first class kit with all types of gears, sprockets, drive chains and even an electric motor. At sea, Margalef made small repairs with a multi-purpose Swiss pocket knife. Unfortunately, probably due to the provisional nature of some of his designs, as well as the general laziness and lack of interest in preserving our history, only a couple of Ramon Margalef’s devices have survived today.

Improving the representativeness of plankton samples was a constant motto for Ramon Margalef since his first studies on marine plankton (Margalef et al. 1952, 1954). The evaluation of phytoplankton biomass, first using as an estimator Harvey’s colour pattern (Harvey units) and later through spectrophotometric analysis of chlorophyll concentration, required robust, efficient and easy-to-use water filtering devices. The designs included systems for filtering a known water volume (originally through home-made collodion filters, as mentioned in the Reuniones de Productividad y Pesquerías) and semi-automatic machines for multiple data collection (Figs 9,10 and 11; Margalef et al. 1952, Margalef 1954 a,b).

After a trial to carry out simultaneous spatial surveys of phytoplankton and physico-chemical variables at series of stations carried out off the coast of Castelló (Margalef and Herrera 1964), the next steps consisted in the design of really complex, semi-automatic multiparameter samplers (the real “rain-making machines”). These were aimed at obtaining simultaneous estimations of environmental variables and phytoplankton and zooplankton data, in order to study the ecological principles responsible for the spatio-temporal patterns observed in phytoplankton biomass and distribution, patch formation and production. The idea was to replace the rigid, time-consuming protocol of classic oceanographic cruises, in which samples were taken at standard depths at fixed stations regularly distributed in transects or grids, with continuous measurements of multiple variables along the ship’s track as it was in motion. This allowed a quasi-synoptic view of the hydrographic structure and its relation to the heterogeneity of plankton distribution to be obtained.

In an initial stage, Margalef (1967d) used optical particle counters to measure seston concentration from sub-surface water samples coming from a continuous water flow with the ship in motion (Fig. 12). Later, starting with the Sahara II cruise on board the Cornide de Saavedra, the equipment for the continuous in situ survey included combinations of continuous automatic measurements of physical parameters (temperature) and chemical parameters (salinity, inorganic nutrients), in a setup that had been implemented by Antoni Ballester (Ballester et al. 1973), with semi-continuous estimates of plankton variables such as photosynthetic pigments, abundance and size-spectrum of suspended particles, water samples for taxonomic phytoplankton analysis, zooplankton abundance (optical plankton counters) and fish biomass (Margalef 1971a). The sampling protocol, which required keeping watches in the long tracks between oceanographic stations, consisted in taking water samples every 15 minutes, reading the sensors, annotating the data that could not be recorded on magnetic or paper tape, controlling the functioning of chemical autoanalysers and other activities, was the subject of jokes among the students who carried it out.

Some of Margalef’s theories required the design of experimental devices contrived to test the effects of particular factors (e.g. temperature, nutrients and turbulence) as drivers of the function and ecophysiology of phytoplankton. The usefulness of laboratory analogues of planktonic ecosystems was thoroughly discussed in Margalef (1956a, 1963b); the devices ranged from the simple culture vessels to compound chemostats, which consisted of serially-connected culture flasks, so that different phytoplankton species would predominate in different flasks according to the division rate of the species and the nutrient flow determining their loss by dilution. Especially noteworthy was the design of the “Helicotrefon”, a phytoplankton culture system consisting of a transparent helical tube installed in a funnel-shaped frame. Nutrients and the phytoplankton inoculum were added at the upper end at a rate calculated to have the maximum phytoplankton concentration at the lower end, where a continuous centrifuge separated cells from the culture medium, which was reused after its nutrient composition had been rectified (Figs 13, 14).

Margalef was also interested in ecophysiological questions that required either mixed or unispecific phytoplankton populations to be maintained under controlled environmental conditions. For his PhD thesis, which aimed to study the effects of temperature on the shape and size of phytoplankton (Margalef 1953a), he designed a system (Fig. 15) in which light, temperature and nutrients could be controlled (Margalef 1954b).

The vertical light gradient and density structure (thermocline) of the oceanic water column was simulated by Margalef in the laboratory using 30 L transparent Perspex cylinders (Fig. 16); in these microcosms, temperature, light and vertical water movement (produced by an oscillating grid attached to a motor) could be automatically controlled, and a small probe allowed fine-scale water sampling for measurements of physical, chemical and biological variables (Margalef 1963a, b). Decades later, this methodology was the inspiration for a fruitful research line at the ICM in relation to the effect of small-scale turbulence on plankton ecosystems (Margalef 1997a, Estrada et al. 1987, Alcaraz et al. 1988, Marrasé et al. 1990, Saiz et al. 1992, Peters et al. 2002, Berdalet et al. 2011).

Margalef’s fascination with nature and his detailed phytoplankton observations were the basis for his contributions to theoretical ecology, and many of his early articles already contain the seed of ideas and concepts that he continued to develop later on. From the beginning, Margalef’s dedication to the examination of phytoplankton was accompanied by an interest in finding regularities and establishing unifying principles. Very soon, he realized the importance of patterns in the number and distribution of species, a field that he had initially developed in relationship with terrestrial communities. Margalef (1949) presented a critique of existing indexes of diversity, which were generally based on adjusting the distribution of the number of individuals of each species to particular mathematical functions. Margalef wanted to find a quantitative expression of diversity that would not depend on previous mathematical assumptions and, in Margalef (1956b), he pointed out the relationship between the richness or specific diversity of a community and the information provided by a sample of this community, and proposed a diversity index based on an expression devised by Brillouin (1951) to define the entropy of a message. This research line matured one year later with Margalef’s opening speech for the Royal Academy of Sciences and Arts of Barcelona, on “Information theory in ecology”, which was published in the reports of the Academy (Margalef 1957f). In this work, Margalef proposed to express diversity by means of an index (H) derived by Shannon and Weaver (1949) to measure the information of a set of symbols (phytoplankton species when applied to plankton) with different a priori probabilities (different frequencies in the case of species). Using some approximations, H and the Brillouin index could be demonstrated to be equivalent, but H was easier to calculate and was more suitable for estimating the diversity of random samples extracted from a community. Though it was published in Spanish and in a country that at that time was not particularly appreciated for its scientific output, “Information theory in ecology” soon attracted international attention, as shown by the appearance of an English translation in the following year (Margalef 1958b). Since then, there have been numerous applications of information theory in ecology and the topic continues to be important today.

The concept of diversity could be applied not only to species numbers but also to traits such as size and biochemical composition. This was the subject of a publication in Scientia Marina (Margalef 1994) based on a contribution to the “NATO Experimental Workshop on the Size Structure and Metabolism of the Marine Microbial Food Web” held in Málaga in 1993. Margalef viewed diversity as a dynamic property, so relationships with other ecosystem characteristics had to be sought in terms of derivatives rather than by considering point values of the variables. For example, biomass would not be directly correlated with diversity, but an acceleration in the production of biomass after a nutrient addition would be associated with a decrease in the first derivative of diversity with respect to time. Margalef also recognized that the idea of species distributions as carriers of information could be applied to spatio-temporal relationships. In this context, he proposed the use of “diversity spectra”, which related species richness or the value of diversity indices to the size or volume of the samples, as ecological descriptors. Reference to the need to consider spatial scales when examining diversity was a constant in Margalef’s publications dealing with this topic (Margalef 1970b, 1972c, 1994).

Margalef’s quest to develop a theoretical framework for ecology was accompanied by an interest in quantitative methods that could help to describe and interpret natural entities, from organisms to ecosystems. He pointed out the insufficiency of routine calculations used at the time in fisheries and oceanography (Margalef 1970a) and searched for new applications of mathematical models and tools, statistical and otherwise. Within this framework, Margalef organized the Seminar of Mathematical Ecology and the Seminar on Factor Analysis in Ecology and Taxonomy, the contributions and discussions of which were published in volumes 34 (1970) and 36 (1972) of Investigación Pesquera. Among the subjects that were discussed in these seminars was network theory (Alvarado and Bonet 1970), currently at the forefront of theoretical ecology developments. Margalef was also interested in mathematical models and one of his early publications in Investigación Pesquera (Margalef 1957c), inspired by research on fisheries, dealt with mathematical functions describing the dispersion of organisms with one or more age classes around a centre (e. g. a breeding centre). Later on, Margalef (1973) pointed out weaknesses of the models of the time, such as the lack of consideration of space, and formulated some principles for the hierarchic construction of models. Margalef (1979), one of his last publications in Investigación Pesquera, used the classical formulation of population changes by means of differential equations to highlight that the condition for population regulation was that inputs (e.g. births and immigration) and outputs (e.g. death and emigration) should be nonlinear functions of the number of individuals, with a higher exponent for outputs.

Margalef’s contribution to Investigación Pesquera, a total of 62 articles, was crucial to shaping the editorial line of this journal and became a pillar of its international recognition (Peters 2010). Scientia Marina, the successor to Investigación Pesquera, was included in the Science Citation Index in the late 1990s and, at present, its impact factor is 1.252 (2018); the journal is completely open access, publishes about 40-50 articles per year and is one of the few that is still managed directly by a scientific institution.

Given the international appreciation achieved by Margalef, a question that has merited comments by his biographers (Peters 2010) is why he wrote so much of his work in Spanish and did not seek to publish in more renowned journals. We must remember that the scientific communication system of the time was different from the present one. It was usual (or even expected) for scientists to publish in the journal of their own institution and, although some journals were more prestigious than others, ranking metrics were not in use. Investigación Pesquera was exchanged with the journals of numerous institutions around the world and the most common way of obtaining an article that was not available in the library was to write to the author requesting a reprint. As suggested by Peters (2010), it is likely that Margalef felt that the language would not be a barrier for interested colleagues. In addition, he surely valued the ability to publish extensive tables of data and to roam into interdisciplinary considerations without editorial constraints. This feeling surfaces in Margalef’s preface to Our Biosphere, a book written on occasion of the 1995 prize of the International Ecology Institute (ECI): “The requirement for laureates to write an EE book provides a welcome opportunity to express oneself more freely than is possible under ordinary publication procedures”.

Reading Margalef’s works through the volumes of Publicaciones del Instituto de Biología Aplicada, Investigación Pesquera and Scientia Marina (Fig. 17) represents a journey through the foundations of marine ecology, first in coastal waters of the Iberian Peninsula and later in some crucial places of the global ocean such as the Caribbean and the upwelling region of NW Africa. In addition to his descriptions of phytoplankton and other marine organisms, a review of the publications of Margalef in these journals allows us to trace how he developed many of his scientific ideas and established a number of unifying principles that continue to inspire current ecological research. The journal Investigación Pesquera, together with its predecessor, Publicaciones del Instituto de Biología Aplicada, and its successor, Scientia Marina, thus constitute the guardians of a fundamental heritage for all marine scientists.