Professional Biologist
Does Scientific Collaboration
Increase the Impact of
Ecological Articles?
ROOSA LEIMU AND JULIA KORtCHEVA
We examined the effects of different types of collaboration on the cilation rates of 837 research papers published in Oecologia/rom 1998 through
2000. Miihiaiithored papers had higher annual citation rates, but also higher self-citation rates, than single-authored papers. Interdisciplinary
collaboration hetween institutioi}s increased citation rates, whereas in-house collaboration reduced them. Contrary to our predictions,
international collaboration had no effect on the citation rates of ecological papers, and US ecologists beneftted from collaboration more than
their European colleagues. Altogether, our results indicate that scientific collaboration in ecology has a rather minor effect on the impact of
the resulting publications, as measured by their citation rates.
Keywords: citation rates, coauthorship, domestic collaboration, international collaboration,
S
cientific collaboration, especially international
and interdisciplinary collaboration, has expanded rapidly
in all fields of research (Avkiran l997,Glanzel2001) and has
become a topic of increasing interest for both scientists and
science policymakers (Moed et al. 1991, Katz and Hicks
1997). Collaboration can be beneficial for several reasons: it
provides a larger pool of available ideas, methods, and resources, and it allows cost sharing and time saving as a result
of division of labor {Avkiran 1997, Katz and Martin 1997).
Consequently, scientific collaboration is commonly considered a prerequisite of higli-quality research, and numerous initiatives by the European Commission and national
governments have been launched with the aim of promoting
collaboration among researchers (Katz and Martin 1997).
The degree of collaboration is also often taken into account
when making funding, hiring, and promotion decisions [Katz
and Martin 1997).
Although scientific collaboration is widely assumed to enhance the quality and impact of scientific research, the evidence for this assumption is contradictory. Using coauthorship
as an indicator of collaboration, several studies have examined the impact of scientific collaboration by comparing the
citation rates of single- and multiauthorcd articles. Citation
frequencies are assumed to indicate the scientific utility of a
study and thus can be used as a partial indicator of study quality and impact (lawani 1986). The number of authors has
been shown to increase the citation rates of individual articles in some disciplines (Abt 1984, Smart and Bayer 1986, Katz
and Hicks 1997, Glanzel 2002, Aksnes 2003), although in
438 BioScience • May 2005 I Yol 55 No. 5
multidisciptinarity
other fields no sucb relationship has been observed {Smart and
Bayer 1986, Avkiran 1997, Rousseau 2001). A critical question
when interpreting the positive relationship between the number of authors and citation rates is whether this pattern reflects a true benefit of collaboration or is due simply to the
increased proportion of self-citations in multiauthored papers (Herbertz 1995) or to the increased probability that
such papers will be brought to the attention of the citer
through personal contacts with at least one of the authors
(Goldfinch et al. 2003). Furthermore, coauthorship is only a
partial indicator of collaboration; it provides no
insight into the precise nature and magnitude of collaboration {Katz and Martin 1997).
The potential benefits of scientific collaboration may
depend on the type of collaboration, the discipline, and the
country or countries involved. For example, international
collaboration is generally considered to increase citation rates
more than domestic collaboration (Narin et al. 1991, Katz and
Hicks 1997, Goldfinch et al. 2003) and to be especially beneficial for scientists from small universities and small or
Roosii ieiiini (e-rmiil: roosa.lrimu&utu.fi)
is a researcber in the Section of
Ecology at the University of Turku, FIN-20014 Turku, Finland. Julia Koricheva
(e-mail: [email protected])
was an academy research fellow in the
Seaiori of Ecology at the University of Turku when this article was prepared;
she is now n lecturer in ecology at the School of Biological Sciences, Royal
HoUoway, University of London, Eglumi, Surrey TW20 OEX, United Kingdom.
© 2005 American Institute of Biological Sciences.
Professional Biologist
remote countries {Rousseau 2001, Goldfinch et al. 2003).
Multi-institutional collaboration has also been shown to increase citation rates, especially if the collaborating Institutions
are from different countries (Narin et al. 1991, Katz and
Hicks 1997, Goldfinch et al. 2003}. In addition, the effect of
collaboration on scientific impact appears to be more positive in the "hard" sciences, such as physics and astronomy, than
in the "soft" sciences, such as sociology (Bridgstock 1991}. If
one accepts that ecology is closer to the soft sciences than to
the hard sciences (Peters 1991), the expected benefits of collaborative research in ecology .should be relatively modest. On
the other hand, the role of interdisciplinary collaboration could
be especially important in ecology; it is an inherently multidisciplinary science, incorporating all the biological disciplines and even nonbiologicalfieldssuch as chemistry, physics,
and geology.
The impact of scientific collaboration on the quality and
visibility ofthe resulting publications has not been explicitly
studied in ecology, although two recent studies have demonstrated that the number of authors affects the probability of
acceptance and the citation rates of ecological papers (Tregenza
2002, Leimu and Koricheva 2005). In the present study we examine the effects of different types and levels of collaboration
on the citation rates of individual research articles to find out
whether some collaboration strategies lead to a greater impact than others. We address the following questions:
• Do the citation rates of ecological papers increase with
the number of authors?
• If so, is this trend due to an increased share of selfcitations in multiauthored papers?
• Do different types of coilaboration (international,
domestic, and in-house) affect citation rates differently?
• Does interdisciplinary collaboration increase citation
rates?
• Are there differences in patterns and benefits of collaboration between US and European ecoiogists?
Literature survey
We examined all articles published in the journal Oecologia
from 1998 through 2000. Oecohgia was chosen for the survey because it is a well-established ecological journal with no
bias as to research topics or plant and animal taxa studied. In
addition, Oecohgia has both European and American editt>rial boards, and has a comparable number of authors from
both North America and Europe. We therefore considered
papers published in Oecologia to be more or less representative of ecological research in general. Furthermore, restricting the scopeof the survey to a single journal eliminates the
journal impact factor as a possible confounding variable in
the analysis. The time span 1998-2000 was chosen because
we were particularly interested in examining the recent
patterns and trends in the infiuence of collaboration on scientific impact. The number of citations did not differ markedly
between the years and ranged from no citations to tens of
citations per paper. Reviews, methodological articles, and
invited contributions for special issues were excludedfi'omthe
analysis. The final data set consisted of 837 research articles.
For each article, we recorded the number of authors, the first
author's country of affiliation, the number of countries and
institutions of affiliation, and the number of biological fields
represented by the authors, as indicated by the names ofthe
departments of affiliation. The last-mentioned variable was
used as an indicator of the interdisciplinarity of collaboration.
The total number of citations received by individual articles
as of July 2004 was obtained from the Science Citation Index,
or SCI, of the Thomson ISI (Institute for Scientific Information). The number of self-citations was calculated by examining the list of authors of each citing article. All citations
for which at least one of the authors of the cited paper was
involved as a coauthor in the citing paper were considered as
self-citations. Annual citation rates and annual self-citation
rates were calculated by dividing the number of citations
and self-citations by the number of years since publication.
Statistical analyses
Wefirstexamined the relationship between the annual citation rates of individual articles, both including and excluding self-citations, and the number of authors, using Pearson's
correlation analysis. To examine the effects of different types
and levels of collaboration on scientific impact, we conducted analyses of covariance to test the effects ofthe number of institutions (one, two, or more), the number of
countries (one, two, or more), and the number of biological
fields (one or more) on the annual citation rates. The number of authors was used as a covariate. Annual citation rates
were log-transformed to meet the assumptions of normal distribution and the homoscedasticity of the variances. The assumption of homogeneous regression coefficients across the
categorical variables was tested by including all possible interactions between the covariate and the categorical variables in the model. None of the interactions was statistically
significant, as required to meet the assumptions of ANCOVA
(analysis of covariance). The results ofthe analysis were the
same regardless of whether self-citations were excluded or included. We therefore present only the results of analyses with
self-citations excluded.
To examine the effect ofthe type of collaboration on scientific impact, we classified collaboration as (a) domestic
in-house collaboration (all authors from the same institution),
(b) domestic multi-institutional collaboration (all authors
from the same country but from more than one institution),
and (c) international collaboration (authorsfi"ommore than
one country), and tested whether annual citation rates differed
among these different levels of collaboration by conducting
an analysis of variance. Annual citation rates were logtransformed to meet the assumptions of ANOVA (analysis of
variance), and self-citations were excluded.
May 2005 I Vol. 55 No. 5 • BioScience 439
Professional Biologist
We further tested whether annual citation rates and selfcitation rates differed between American and European
authors by conducting one-way ANOVAs. To test whether the
influence of collaboration on scientific impact varied
between American and European authors, we conducted
separate ANCOVAs for American and European authors and
tested the effects of the number of countries, the number of
institutions, and the number of biological fields on annual
citation rates using the number of authors as a covariate.
Citatioti rates were log-transformed to meet the assumptions (of normal distribution and of the homoscedasticity of
the variances), and self-citations were excluded.
To test for possible national differences in citation patterns
(Moller 1990,Wardle 1995), we selected from our data set 15
papers by US ecologists and 15 by European ecologists. These
papers were randomly selected from those whose authors all
came fTom the same country. For the European papers, tbe
sample included papers authored by researchers from nine different countries; the countries included, and the number of
papers per country, were chosen to reflect the relative frequency of papers by researchers from these countries published in Oecologia. For the articles selected, we checked all
papers that were cited in them and selected tbose tbat were
available in the ISI database. We counted the proportion of
US and European papers cited in each of the papers and
tested the difference between these proportions separately for
American and European ecologists, using Kruskal-Wallis
nonparametric tests. The percentage of citations to American
or European authors of the total ISI citations per paper was
used in the analysis.
Results of the survey
We found that 85 percent of the papers published in Oecologia ffom 1998 through 2000 were multiauthored (82 percent
of US papers and 86 percent of European papers); authors
from more than one institution were involved in 41 percent
of the papers, and 19 percent of the papers were written by
authors from more than one country. While the frequency of
multi-institutional collaboration was the same in US and
European studies, European ecologists collaborated with
researchers ffom other countries much more frequently (27
percent of the papers) as compared to the US ecologists {10
percent). The mean numhers of authors, institutions, and
countries per paper were 2.8 (± 1.6), 1.6 (± 0.9), and L2
(± 0.5), respectively. The average number of authors per paper was slightly higher in European studies {3.1 ± L8) than
in US studies (2.5 ± L3). Authors represented more than one
biologicalfield{as indicated by the names of their departments
of affiliation) in 18 percent of the papers, and the frequency
of interdisciplinary collaboration was similar in US and European studies {18.3 percent and 17.7 percent, respectively).
The mean annual citation rate of the papers was 2.4 (± 2.3),
and self-citations accounted for 25 percent of all citations.
Overall, no differences were found in annual citation rates
between US and European authors {US: 2.6 ±0.16; European:
2.3 ± 0.10; F - L21, df = 1, P - 0.271), but annual self-
440 BioScience • May 2005 / Vol. 55 No. 5
citation rates were found to be significantly lower for papers
authored by Americans than for those by Europeans (US: 0.56
± 0.03; European: 0.63 ± 0.04; F -5.09, df - 1, P = 0.024).
When self-citations were excluded ffom the analysis, the annual citation rates of papers by US authors were significantly
higher than those of Europeans (US: 2.01 ±0.14; European:
1.68 ± 0.08; F - 4.82, df = 1, P - 0.028).
Annual citation ratej. correlated positively with the number of authors, whether self-citations were included (r - 0.16,
P ^ 0.0001) or excluded [r = 0.09, P ^ 0.009; figure 1), although
in the latter case the relationship was very weak. Pearson's correlation coefficient between annual self-citations and the
number of authors was also significantly positive (r - 0.274,
P= 0.0001; figure 1). Annual citation rates increased statistically significantly with the number of authors for both
US (r - 0.220, P = 0.0001) and European studies {r - 0.133,
P = 0.0148). When self-citations were excluded, however, the
positive relationship between number of authors and citation
rate was significant for US studies only (r= 0.166, P - 0.0016).
Neither the number of countries nor the number of biological fields affected the annual citation rates of papers by
either European or US ecologists (table 1). However, the
number of institutions had a statistically significant effect on
the annual citation rates of all studies and European studies,
and there was a significant interaction between the number
of institutions and the number of biological fields involved
in the collaboration in all the analyses (table 1). The number
of biological fields increased citation rates only when multiple institutions were involved in the collaboration (figure 2).
On the other band, when only one institution was involved,
the number of biological fields decreased citation rates (figure 2). The level of collaboration (domestic in-house, domestic
multi-institutional, or international) did not affect annual
citation rates (all papers: F = 1.21, df = 2, P - 0.298; US:
P= 0.77,df- 2 , P - 0.462; Europe: F - 0.27,df- 2,P= 0.761;
figure 3).
We found that US ecologists cite papers written by their
compatriots (69.8 percent of ISI citations) more ffequently
tban those by European ecologists (15.5 percent) (x^= 18.6,
df - 1, P = 0.0001). European ecologists, on the other hand,
were found to cite US (47.1 percent) and European papers
(36.4 percent) with nearly equal frequency ( x ' - 1.17,df- 1,
P-0.280).
Discussion and conclusions
A vast majority of the papers examined were multiauthored,
indicating that scientific collaboration plays an important role
in ecology. Multi-institutional and international collaboration
was also common, and the percentage of internationally authored articles in Oecologia was similar to or higher than the
percentages previously reported for biology (Moed et al.
1991, Luukkonen et al. 1992) and freshwater ecolog)' (Resh
and Yamamoto 1994). In accordance with previous studies in
ecology (Leimu and Koricheva 2005) and in other disciplines
(Abt 1984, Glanze! 2002), we found that citation rates of
ecological papers increased with the number of authors, and
Professional Biologist
this increase was especially pronounced when the number of
authors exceeded four (figure 1), For the European studies,
this relationship was simply the result of an increase in the
number of self-citations in muhiauthored pubhcations
(cf Herbert/ 1995). In the US studies, on the other hand, the
correlation between citation rates and number of authors remained significant after self-citations were excluded from
the analysis. The higher citation rates of multiauthored
papers may be due to higher quality of the collaborative
research, to enhanced dissemination in the research community through the personal communications of many
authors, or both (Aksnes 2003, Goldfinch et al. 2003).
When self-citations were excluded from the analysis, and
variation in the number of authors was accounted for by
means of ANCOVA, the benefits of collaboration in terms of
increased citation rates were relatively minor and did not
differ among various forms of collaboration (in-house,
domestic, and international). Perhaps the most interesting and
intriguing finding of our study, which was true for both
US and European papers, is the interactive effect of multiinstitutional and interdisciplinary collaboration on citation
rates. We found that interdisciplinary collaboration enhances
the citation rates of ecological studies only if more than two
institutions are involved. Collaboration between departments
within the same institution, on the other hand, significantly
reduces citation rates compared with those of research conducted within the same department. A somewhat similar
phenomenon at the institutional level has recently been reported by Cloldfinch and colleagues (2003), who found that
an increase in the number of domestic institutions involved
in collaboration reduced the citation rates of articles by scientists from New Zealand. Taken together, these findings
suggest that collaboration with one's nearest neighbors (a kind
of "scientific inbreeding") may actually reduce the impact and
visibility of the resulting publications.
Interestingly, althougb international collaboration has
been viewed as an especially important prerequisite of bighimpact research (Narin et al. 1991, Aksnes 2003), we found
that the number of countries involved in the collaboration had
no significant impact on the annual citation rates of either
European or US ecological articles. It thus seems that international collaboration does not markedly enhance the scientific impact of ecological papers published in Oecologia.
Previous studies that have reported higher citation rates for
internationally authored papers were usually restricted to
studies conducted within a single country, but included publications in different journals (Narin etal. 1991, Katz and Hicks
1997, Rousseau 2001, Aksnes 2003, Coldfmch et al. 2003). It
has been shown that in several countries internationally
coauthored papers are published in journals with different impact factors from those that publish domestic papers (Glanzel
2001). The different citation rates previously reported for
internationally and nationally authored papers could thus be
due to these studies' publication in different journals; our
study, on the other hand, demonstrates that within a single
specific journal there may be no significant difference in
citation rates between the two categories of studies.
The observed lack of benefits of international collaboration may also be partly due to the general globalization of science. Scientists from different countries are nowadays more
closely connected, and the availability and exchange of information and knowledge continue to expand. As differences have decreased between the scientific impact of nations
(King 2004), the effect ot international collaboration may have
diminished as well. It has been shown, for instance, that in the
4.0
—•— Total citations
3.5
• -* - Self-citations
—•- Citations by others
3,0
2.5
1
^
•
2.0
1.5
1.0
0.5
0.0
3
4
5
Number of authors
Figure I. Reiationship between the number of authors
per paper and annual citation rates.
Table 1. Effects ofthe number of institutions, countries,
and bioiogica! fields involved in the collaboration of
ecological papers on annual citation i ates.
Variable
All papers
Number of institutions
df
F
P
2
2
0.0224
0.2276
0.3389
0.0025
Number of biological fields
1
Number of institutions x
number of biological fields
2
3.82
1.48
0,92
6,03
Number of countries
Number of authors
1
5.25
0,0222
European papers
Number of institutions
2
Number of countries
2
Number of biological fields
1
Number of institutions x
number of biological fields
2
3.29
0.99
0.91
4.12
0.0386
0.3740
0.3415
0.0171
Number of authors
1
2.34
0.1270
US papers
Number of institutions
2
Number of countries
2
0.2367
0.9291
0,8297
0.0367
0.1088
Number of biological fields
1
Number of institutions x
number of biological fields
2
1.45
0,07
0.05
3.34
Number of authors
1
2.58
Note: Results are from ANtXWA (analysis of covariance 1 with
number of authors as a covariate; self-citations are excluded from the
analysis.
May 2005 / Vol. 55 No. 5 • BioScience 441
Professional Biologist
early 1980s, internationally coauthored articles received significantly more citations than domestic articles, but in the late
1990s, international collahoration increased citation rates
compared with those of domestic collaboration only when
more than three authors were involved (Persson et al. 2004).
Since our data set consists only of recent papers, it is not
possible to test whether the importance of international collaboration has diminished in recent years in ecology as well.
2.5
• One biological field
• Two or more biological fields
2,0
1.5
1.0
0,5
0.0
>3
Institutions
Figure 2. Impact of study multidisciplinarity (the number
of biological fields represented by the authors, as indicated by the names ofthe departments of affiliation), and
ofthe number of institutions involved in a study, on annual citation rates (self-citation excluded). Graph shows
least-square means adjusted for the number of authors.
The vertical line at the top of each bar represents standard error.
Internationa!
Domestic
In-house
Figure 3. Effects of type of collaboration on annual citation rates of papers by US and European ecologists.
442 BioScience • May 20051 Vol. 55 No. 5
On average, European ecologists seem to be more collaborative than US researchers: the proportion of multiauthored
papers, the average number of authors per paper, and especially the proportion of internationally coauthored papers were
higher for European studies than for US ones. This is as expected; researchers from smaller countries are assumed to be
in greater need of collaboration (Goldfinch et a!. 2003). However, the greater coilaboration efforts of European ecologists
do not translate into larger benefits in terms of increased citation rates of their articles as compared with those produced by the American researchers. On the contrary, US
ecologists seem to benefit from cooperation more than European ecologists do; the citation rate of the US papers was
positively correlated with the number of authors and tended
to be higher for internationally authored papers (figure 3}.
In agreement with our previous study (Leimu and
Koricheva 2005}, we also found that studies by US authors
were more frequently cited on average than those by European
ecologists. This was not due to a higher proportion of selfcitations in US studies; on the contrary, papers by US authors
received fewer self-citations than those by Europeans. On
the other hand, we found that US ecologists preferentially cite
US papers, whereas European ecologists cite US and European
authors equally often (cf. Moller 1990, Wardle 1995}. Two
alternative explanations of this pattern are possible. Either
citation practices of US researchers are parochial and inflate
the citation rates of US papers, given the large US share of publications (King 2004), or papers by US authors are of higher
quality, which is recognized by US ecologists, whereas it is the
European ecologists who are parochial as they frequently
cite the inferior European papers. We were unable to distinguish between these alternatives, because judging the quality
ofthe studies Is problematic, and this topic is beyond the scope
of the current study.
Overall, our study has shown that scientific collaboration
in ecology has a fairly minor, and not always positive, effect
on the citation rates of the resulting publications. Similar
conclusions have been reached by studies in several other fields
(HerbertzandMuiler-Hill 1995,Avkiran 1997). On the other
hand, Tregenza (2002) has shown that single-authored papers
have a higher probability of being rejected by ecological journals than multiauthored ones. Oecologia is one of the major
ecological journals and has a rigorous refereeing process,
with only 20 percent of the submitted manuscripts being
accepted for publication. It is thus possible that ecological studies involving different degrees of collaboration vary in quality at the submission stage, but that no differential in quality
remains after the refereeing process. Furthermore, citation rates
measure only scientific utility and not other aspects of study
quality, such as methodological quality and originality. Future
studies should examine the impact of scientific collaboration
in ecology on these aspects as well. Until evidence of such an
impact is found, however, decisionmakers should be cautious about assigning too much importance to the presence
of scientific collaboration in the allocation of research funds.
Professional Biologist
Acknowledgments
We are grateful to Ellen Valle for checking the language of this
paper. The study has been financially supported by the Academy of Finland.
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