The Impact of Lynn Margulis as seen through a Citationist perspective

 

A.I.Pudovkin¹, E.Garfield²

 

¹Institute of Marine Biology, Vladivostok, Russia, e-mail: aipud@mail.ru

²ThomsonReuters Professional, Philadelphia, PA 19130-4067,

   e-mail: eugene.garfield@thomsonreuters.com

 

My co-author Dr. Garfield has asked me to convey his regrets that he could not be present today. The last time he  saw Lynn Margulis was in Barcelona where she and Ricardo Guerrero introduced him to a wonderful tapas restaurant. He first met Dr. Margulis many decades ago at a time long forgotten.  They had a significant connection through a mutual friend -- Miriam Balaban -- the original publisher of the journal “Symbiosis”  of which Lynn was the editor. It is an honor for us to say a few words about her influence on science, but from the outset we  must admit that we know very little about her work. What follows we have been able to derive from the data base most familiar to us and known to most of you as the Science Citation Index (SCI)  or in its more recent electronic form the Web of Science.(WOS)

 

We have to make the assumption that you are familiar with SCI or WOS. Very briefly, the WOS permits you to find the papers published by any author over the past century but the journal literature covered by this database is especially comprehensive since the end of World War II. Since Lynn Margulis published mainly in well-known journals the WOS search is complete as far as we could determine. In the discussion that follows we will discuss her approximately 300 papers and books as well as that much larger journal literature (5600 papers) in which her work has been cited. The former is first mainly identified in the WOS Source Index. The latter is identified in the main section of WOS called the citation index or cited references index. For each paper listed in the Source Index one finds the traditional bibliographic citation consisting of the article title, journal title and date as well as the authors and their addresses. However, unlike traditional bibliographies each WOS entry contains the complete list of books or journal articles cited by the authors. This list of cited references is essential to the creation of the Historiographs which are the main theme of this presentation.

 

For the past few years the WOS has been augmented by the addition of a software package called HistCite. This software is available free of charge to any user of the WOS. HistCite was originally created by us (E.Garfield , A.I. Pudovkin and V.S. Istomin).

 

To create a HistCite collection one must first perform a search of WOS. Having found the approximately 250 papers published by Margulis, the collection of bibliographic citations is downloaded to HistCite. It is possible to add publications to the HistCite collection that are not included in WOS. We have done that for many of the items in this collection. Many of these non-WOS publications are found in the literature cited by Margulis or other authors.

 

The second and perhaps most important part of this exercise is to find the collection of papers citing Lynn’s work. We performed a  “Citation Search” in WOS and exported the WOS entries for these citing papers  including all the references  cited in each paper. To this much larger collection of 5600  citing papers we added  the first collection of Margulis’s own publications.

Thus, we have 2 collections: 1) Publications by L Margulis, 259 papers; we call it the 1^st collection; 2) Margulis & the citing papers, 5593 papers; we refer to it as the 2^nd collection.

 

Having considered the both collections one can summarize Lynn Margulis’s publication activity: she had 259 publications, which appeared in about 100 journals, from 1958 to 2010 and were cited by 5593 papers. Lynn had 192 co-authors, the 10 most frequent ones are listed in Table 1. Lynn authored and co-authored a few books, some of which were highly cited. They are listed in Table 2. Table 3 shows her most cited publications. The five most frequent words in the titles of her papers clearly characterize the topic of her research. These words are EVOLUTION (34), ORIGIN (26), MICROBIAL (23), LIFE (21), SYMBIOSIS (16); in parentheses are shown the numbers of occurrences out of the overall number of 872 words.

 

Table 4 shows 10 most cited Lynn’s publications ranked by LCS rather than by GCS (as in Table 3). One can see considerable discrepancy between the two rankings, which shows the difference of importance of papers for the peers working in the same science field and for the more general community of scientists. Table 5 lists  4 papers showing the greatest differences in LCS and GCS rankings. Understandably, books of a more popular kind (Margulis L, Schwartz KV. 1988. Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth; Margulis L; Fester R. 1991. Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis) are ranked considerably higher by the general scientific community than by specialists in the field. While papers of a narrower, specialized character (see Table 5) are ranked higher by specialists than by the general scientific community.

 

It is interesting to mention that the 17 papers, mostly of a philosophical or popular scientific kind, Lynn wrote were in co-authorship with her son, Dorion Sagan.  He is a well-known science writer, essayist, and theorist, who has written many books on culture, evolution, and the history and philosophy of science.

 

An important feature of HistCite is the ability to automatically create map-like graphs, which we term historiographs.  A historiograph shows the citation links between the various papers shown in the graph. Now let us consider two historiographs for the 1st collection (that is for Margulis’s own on papers).  Historiograph 1G1 (Fig.1) shows the citation links among the top 30 papers sorted by Local Citation Score (LCS). These papers (or nodes) were published from 1967 to 2006.  LCS is the number of citations of a paper by the ones within the collection, while Global Citation Score (GLS) is the number of cites a paper gets within the global WOS.  Each node (circle) in the graph corresponds to a paper. The size of the node is proportional to citation numbers (LCS or GCS).

 

In the  historiograph  1G1 one can see 2 chronological distinct clusters: a) papers of 1967-1988; b) papers of 1990-2006. These 2 clusters are interconnected only through one 1986 paper, node #117. We cannot say why Lynn did not cite her earlier papers in her later works. Possibly, her interest shifted from the origin of
eukaryotic cells, which is discussed in the first cluster of papers, to the problems of phylogeny and evolution of different microorganism taxa discussed in the 2^nd cluster. Though, on scanning the titles of the papers one sees considerable overlap in the topics in both clusters. It can be seen that Lynn cites her books more frequently than she cites her journal papers.

Historiograph 1G2 (Fig.2) shows the top 40 papers (of the same 1^st collection) sorted by GCS (which takes into account not only citations by Margulis but all papers in the WOS collection). This graph does not show any clear-cut clusters. Though the same tendency can be seen here as well: papers of 1990 and later do not cite earlier ones. It is clearly seen in the graph, that Lynn’s books are cited much higher than her journal papers.

 

Now  let’s consider the 2nd collection, that is,  the 5593 citing papers including those by Margulis. Table 6 shows the 5 most globally cited papers of the 2^nd  collection. One can see that the papers, which cited papers by Margulis, were most authoritative, highly impact papers. This is indirect though convincing evidence of the impact and significance of Lynn Margulis’s papers.

 

Table 7 lists some authors, frequently citing Margulis’s papers (see column A) and who are themselves globally highly cited authors (see column D). All these authors are well-known authorities in the field of evolutionary biology -- experts and theorists on the problems of early biological evolution and  on the origin of the eukaryotic cell. To better understand these data let’s consider the 2^nd line, data on Doolittle DF. This very well-known author cited Lynn Margulis in 33 of his papers (column A), which were cited by 506 papers of the “citing collection” (column B). This speaks about the importance of Margulis’s papers for Doolittle and the importance of Doolittle’s papers for the authors of the “citing collection”, that is for the scientists who work in the same field as Margulis and cite her papers. The high status of DF Doolittle is characterized by his very high overall citation (15,079, see column D), high average citation of his papers (54.6, column E) and high h-index (62, column F). Similarly, the 11^th line gives data on Woese CR -- another top cited author (his overall citation number is 39,367; see column D). This author published 254 papers, 16 of which cited Lynn’s publications  (column A), which says that his research scope does not fully coincide with that of Lynn’s publications. However, these 16 papers by Woese were cited by 984 papers of the collection (column B). This provides evidence of the interest of Lynn’s papers for Woese and the importance of these 16 papers for the other citing authors of the collection.

 

Again, HistCite has generated  two historiographs for this collection, which we will denote  as 2G1 (Fig.3; 30 most cited  papers  by LCS) and 2G2 (Fig.4; 35 top papers scaled by GCS). In the historiograph 2G1 one sees the main Margulis’s publications (17 in this graph, both journal papers and books) and the citation links among them plus publications by other authors dedicated to the same topics. There are no time clusters here, which were seen in the similar graph for the 1^st collection. Though specific citation patterns of Lynn is also discernible here: she prefers to cite her recent publications rather than older ones. Let’s consider the node 2709 (Margulis L. 1996. Archaeal-eubacterial mergers in the origin of Eukarya: Phylogenetic classification of life. PNAS, 93 (3): 1071-1076). This paper cites  4 of her publications, but all of them were published later than 1986; citing her own books, she cited only the latest editions, thus making the citation pattern “time-shallow”.

 

In the historiograph 2G2 one sees highly cited (globally) publications of different authors on diverse problems of microbiology, biochemistry, etc., some of which are only tangentially related to the main interests of Lynn Margulis. For instance, node 3094 (Green DR, Reed JC. 1998. Mitochondria and apoptosis. Science, 281:1309-1312).  It is the top cited paper within the collection, GCS 5328, though LCS is only 14, this paper cites only 1 paper by Margulis (1996,PNAS, 93: 1071). There are only 2 publications by Margulis in this graph, both are books (Origin of Eukaryotic Cells, 1970; Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons, 1981). The graph is dominated by highly cited publications by Woese CR (nodes 555, 817, 1529, 1993, 2394). The papers of this author are both highly locally cited (within the collection) and highly globally cited (in WOS)

 
For the both collections the historiographs showing the most locally cited
papers (1G1 and 2G1) are more meaningful compared to those, which  show  globally well  cited papers (1G2 and 2G2). We mean that historiographs created for the sets of papers with the highest LCS are more structured, easier to interpret. That publications with highest LCS are more relevant, more topically related to the collection. The ability to identify the most locally cited (or locally citing) papers is a unique feature of HistCite, not available in WOS.

Table 1.  Ten most frequent co-authors of Lynn Margulis

 

Recs is the number of papers co-authored with L.Margulis, TLCS (total local citation score) is the summary number of cites from the papers within the collection, TGCS (total global citation score) is the summary number of cites the author’s papers in the collection got in the WOS.

 

 

 

Table 2.  Books by Lynn Margulis. 

 

TGCS is the total global citation score.

 

 

	Authors	Title	Year Published	Further editions	TGCS
1	Margulis L	Origin of Eukaryotic Cell	1970		958
2	Margulis L	Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons	1981	1993	1067
3	Margulis L, Schwartz KV	Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth	1982	1988 1998	447
4	Margulis L, Sagan D	Microcosmos: Four Billion Years of Evolution from Our Microbial Ancestors	1986		121
5	Margulis L, Sagan D	Origins of Sex: Three Billion Years of Genetic Recombination	1986		102
6	Margulis L, Fester R.	Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis	1991		183
7	Margulis L, Sagan D	What Is Life?	1995		83
8	Margulis L	Symbiotic Planet: A New Look at Evolution	1998		119
9	Margulis L, Sagan D	Acquiring Genomes: A Theory of the Origins of Species	2002		108

 

Table 3 Ten most cited (globally) publications by lynn Margulis.

LCS is Local citation score, GCS is GCS is Global Citation Score, LCR is Local Cited References, CR is Cited References

#	Date / Author / Journal	LCS	GCS	LCR	CR
1	17 MARGULIS L Origin of Eukaryotic Cells ORIGIN EUKARYOTIC CE. 1970;	15	958	0	0
2	87 MARGULIS L Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons SYMBIOSIS CELL EVOLU. 1981;	21	794	0	0
3	169 MARGULIS L Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons SYMBIOSIS CELL EVOLU. 1993;	19	273	0	0
4	146 MARGULIS L, Corliss JO, Melkonian M, Chapman DJ Handbook of Protoctista: The Structure, Cultivation, Habitats and Life Histories of the Eukaryotic Micro-organisms and Their Descendants Exclusive of Animals, Plants and Fungi HDB PROTOCTISTA. 1990;	23	219	0	0
5	4 MARGULIS L ON ORIGIN OF MITOSING CELLS JOURNAL OF THEORETICAL BIOLOGY. 1967; 14 (3): 225-&	8	203	1	81
6	158 MARGULIS L, Fester R Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis SYMBIOSIS SOURCE EVO. 1991;	3	183	0	0
7	88 MARGULIS L, Schwartz KV Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth 5 KINGDOMS ILLUSTRAT. 1982;	8	181	0	0
8	133 MARGULIS L, Schwartz KV Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth 5 KINGDOMS ILLUSTRAT. 1988;	4	154	0	0
9	26 MARGULIS L COLCHICINE-SENSITIVE MICROTUBULES INTERNATIONAL REVIEW OF CYTOLOGY-A SURVEY OF CELL BIOLOGY. 1973; 34: 333-361	12	150	7	111
10	186 Margulis L Archaeal-eubacterial mergers in the origin of Eukarya: Phylogenetic classification of life PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 1996 FEB 6; 93 (3): 1071-1076	7	141	6	46

Table 4.  Ten papers by Lynn Margulis, most frequently cited by herself. Column heads are as in Table 3.

#	Date / Author / Journal	LCS	GCS	LCR	CR
1	146 MARGULIS L, Corliss JO, Melkonian M, Chapman DJ Handbook of Protoctista: The Structure, Cultivation, Habitats and Life Histories of the Eukaryotic Micro-organisms and Their Descendants Exclusive of Animals, Plants and Fungi HDB PROTOCTISTA. 1990;	23	219	0	0
2	87 MARGULIS L Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons SYMBIOSIS CELL EVOLU. 1981;	21	794	0	0
3	169 MARGULIS L Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons SYMBIOSIS CELL EVOLU. 1993;	19	273	0	0
4	17 MARGULIS L Origin of Eukaryotic Cells ORIGIN EUKARYOTIC CE. 1970;	15	958	0	0
5	26 MARGULIS L COLCHICINE-SENSITIVE MICROTUBULES INTERNATIONAL REVIEW OF CYTOLOGY-A SURVEY OF CELL BIOLOGY. 1973; 34: 333-361	12	150	7	111
6	11 NEVIACKA.JA, MARGULIS L EFFECT OF COLCHICINE ON REGENERATING MEMBRANELLAR CILIA IN STENTOR COERULEUS JOURNAL OF PROTOZOOLOGY. 1969; 16 (1): 165-&	11	23	0	26
7	23 YOUNGER KB, WINSTON M, BANERJEE S, MARGULIS L, KELLEHER JK EVIDENCE THAT SYNCHRONIZED PRODUCTION OF NEW BASAL BODIES IS NOT ASSOCIATED WITH DNA-SYNTHESIS IN STENTOR-COERULEUS JOURNAL OF CELL SCIENCE. 1972; 11 (2): 621-&	10	28	3	40
8	129 BERMUDES D, MARGULIS L, TZERTZINIS G PROKARYOTIC ORIGIN OF UNDULIPODIA - APPLICATION OF THE PANDA PRINCIPLE TO THE CENTRIOLE ENIGMA ANNALS OF THE NEW YORK ACADEMY OF SCIENCES. 1987 JUL 9; 503: 187-197	10	14	9	62
9	178 KIRBY H, MARGULIS L KIRBY,HAROLD SYMBIONTS OF TERMITES - KARYOMASTIGONT REPRODUCTION AND CALONYMPHID TAXONOMY SYMBIOSIS. 1994; 16 (1): 7-63	10	19	2	33
10	24 BANERJEE S, WINSTON M, KERR V, KELLEHER JK, MARGULIS L MELATONIN - INHIBITION OF MICROTUBULE-BASED ORAL MORPHOGENESIS IN STENTOR-COERULEUS JOURNAL OF PROTOZOOLOGY. 1972; 19 (1): 108-&	9	45	4	24

 

 

Table 5.  Papers by Lynn Margulis, which have maximal difference in ranking by LCS and GCS

 

R_LCS is the rank by LCS, R_GCS is the rank by GCS, ∆ is the difference between the ranks.

 

	Paper	RLCS	RGCS	∆
1	129 BERMUDES D, MARGULIS L, TZERTZINIS G PROKARYOTIC ORIGIN OF UNDULIPODIA - APPLICATION OF THE PANDA PRINCIPLE TO THE CENTRIOLE ENIGMA ANNALS OF THE NEW YORK ACADEMY OF SCIENCES. 1987 JUL 9; 503: 187-197	8	77.5	69.5
2	178 KIRBY H, MARGULIS L KIRBY,HAROLD SYMBIONTS OF TERMITES - KARYOMASTIGONT REPRODUCTION AND CALONYMPHID TAXONOMY SYMBIOSIS. 1994; 16 (1): 7-63	9	62.5	53.5
3	158 MARGULIS L, Fester R Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis. 1991.	66	6	60.0
4	133 MARGULIS L, Schwartz KV Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth. 1988.	47	8	39.0

 

Table 6. Five most cited papers, citing Lynn Margulis’s papers.

 

#	Date / Author / Journal	LCS	GCS	LCR	CR
1	3094 Green DR, Reed JC Mitochondria and apoptosis SCIENCE. 1998 AUG 28; 281 (5381): 1309-1312	14	5328	4	56
2	1529 WOESE CR BACTERIAL EVOLUTION MICROBIOLOGICAL REVIEWS. 1987 JUN; 51 (2): 221-271	225	4390	20	284
3	1893 WOESE CR, KANDLER O, WHEELIS ML TOWARDS A NATURAL SYSTEM OF ORGANISMS - PROPOSAL FOR THE DOMAINS ARCHAEA, BACTERIA, AND EUCARYA PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 1990 JUN; 87 (12): 4576-4579	178	2432	7	33
4	1045 YANCEY PH, CLARK ME, HAND SC, BOWLUS RD, SOMERO GN LIVING WITH WATER-STRESS - EVOLUTION OF OSMOLYTE SYSTEMS SCIENCE. 1982; 217 (4566): 1214-1222	3	1997	1	100
5	555 WOESE CR, FOX GE PHYLOGENETIC STRUCTURE OF PROKARYOTIC DOMAIN - PRIMARY KINGDOMS PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 1977; 74 (11): 5088-5090	147	1245	4	32

 

Table 7.  Citation characteristics of authors, frequently citing papers by Lynn Margulis.

 

A is number of records in the 2^nd  Margulis collection; B is the Total Local Citation Score; C is the global number of records (in WOS); D is the global (in WOS) number of cites; E is the average number of cites per paper; F is the h-index.