Ecology Letters, (2020) doi: 10.1111/ele.

13664

REVIEW AND
SYNTHESIS Uncovering patterns of freshwater positive interactions using
meta-analysis: Identifying the roles of common participants,
invasive species and environmental context

Lindsey K. Albertson, Michael
J. MacDonald, Benjamin B.
Tumolo, Michelle A. Briggs,
Zachary Maguire, Sierra Quinn,
Jose A. Sanchez-Ruiz, Jaris Veneros
and Laura A. Burkle
Department of Ecology, Montana
State University, P.O. Box 173460,
Bozeman, MT 59717, USA
*Correspondence: E-mail: lindsey.
albertson@montana.edu
Abstract
Positive interactions are sensitive to human activities, necessitating synthetic approaches to eluci-
date broad patterns and predict future changes if these interactions are altered or lost. General
understanding of freshwater positive interactions has been far outpaced by knowledge of these
important relationships in terrestrial and marine ecosystems. We conducted a global meta-analysis
to evaluate the magnitude of positive interactions across freshwater habitats. In 340 studies, we
found substantial positive effects, with facilitators increasing beneficiaries by, on average, 81%
across all taxa and response variables. Mollusks in particular were commonly studied as both
facilitators and beneficiaries. Amphibians were one group benefiting the most from positive inter-
actions, yet few studies investigated amphibians. Invasive facilitators had stronger positive effects
on beneficiaries than non-invasive facilitators. We compared positive effects between high- and
low-stress conditions and found no difference in the magnitude of benefit in the subset of studies
that manipulated stressors. Future areas of research include understudied facilitators and benefi-
ciaries, the stress gradient hypothesis, patterns across space or time and the influence of declining
taxa whose elimination would jeopardise fragile positive interaction networks. Freshwater positive
interactions occur among a wide range of taxa, influence populations, communities and ecosystem
processes and deserve further exploration.

Keywords
Ecosystem engineering, facilitation, habitat modification, mutualism, resource subsidy.

Ecology Letters (2020)

modification, protection and transport (Jones et al., 1994;

INTRODUCTION
Biotic interactions fundamentally influence populations, com-
munities and ecosystem processes. A growing need to under-
stand biotic interactions stems from their potential to be
altered by human activities, including climate warming (Pre-
ston et al., 2008; Montoya and Raffaelli, 2010; HilleRisLam-
bers et al., 2013). Additionally, biodiversity loss and invasive
species alter biotic interactions, leading to cascading influences
on important ecosystem functions (Estes and Duggins, 1995;
Mooney and Cleland, 2001; Angelini et al., 2011). Although
positive biotic interactions play key roles (Brontstein, 2015),
they have received far less synthetic attention than negative
biotic interactions such as competition and predation (Menge
and Sutherland, 1987; Gurevitch et al., 2001; Chesson and
Kuang, 2008). At the turn of the century, several reviews
highlighted the importance of positive interactions (Fig. 1;
Stachowicz, 2001; Bruno et al., 2003), yet many questions and
areas for improved understanding still remain, including
quantifying positive interaction magnitude and investigating
patterns across taxa, life-history stage and habitat type (Bert-
ness and Callaway, 1994; Callaway and Walker, 1997; Jones
et al., 1997; Choler et al., 2001; Trautz et al., 2017).
Positive biotic interactions such as facilitation, mutualism
and commensalism can be supported by several direct and
indirect mechanisms, including habitat modification, resource
Bertness and Leonard, 1997; Subalusky and Post, 2019).
Understanding the relative strength of positive interactions
across mechanisms, facilitator and beneficiary identity, inva-
sion status, space and time has been a central goal of many
researchers in this field over the past several decades. For
example, differences in mechanisms of habitat modification
(e.g. organismal structures such as coral reefs) versus resource
modification (e.g. breakdown of leaf material by organisms
such as aquatic invertebrates) help explain the relative
strength of positive interactions across space and time (Wright
and Jones, 2006; Hastings et al., 2007; Tumolo et al., 2020).
Additionally, positive interactions have been documented as
critical components of many pairwise or network interactions
that can even modify competitive or predatory relationships
(Losey and Denno, 1998; Kay and Schemske, 2004; Gross,
2008; Thomsen et al., 2010). Organisms that facilitate others,
especially through the mechanism of habitat modification (i.e.
ecosystem engineers), are increasingly used for restoration and
can be disproportionally influential when they are lost from
ecosystems or displaced by invasive species that disrupt net-
work interactions (Crooks, 2002; Crain and Bertness, 2006;
Halpern et al., 2007; Renzi et al., 2019).
It has been challenging to establish general patterns and
context-dependency of positive interactions (Maestre et al.,
2006; Silliman and He, 2018), but progress in our

© 2020 John Wiley & Sons Ltd

2 L. K. Albertson et al.
understanding in terrestrial and marine environments has far
outpaced that in freshwater ecosystems (Bertness and Call-
away, 1994; Callaway et al., 2002; Morris et al., 2007). In ter-
restrial and marine ecosystems, positive interactions are well
recognised to regulate ecosystem function and biodiversity
and have provided important evidence to test central concepts
in ecology (Schemske et al., 2009; Angelini et al., 2011; He
et al., 2013; Bulleri et al., 2016). For example, positive interac-
tions in soils explain patterns of biodiversity and dispersal of
microbes from above to below ground (Wardle, 2006). In
marine ecosystems, positive interactions are related to
increases in biodiversity (Hacker and Gaines, 1997). Addition-
ally, positive interactions in both marine and terrestrial
ecosystems can explain niche space expansion, which ulti-
mately has implications for ecosystem functions and services
(Bulleri et al., 2016). A recent review highlighted myriad ways
that positive interactions occur in freshwater ecosystems
across plant and animal taxa (Silknetter et al., 2020). For
example crayfish feeding and burrowing activity facilitates
benthic algal species and macroinvertebrate density, often in
sediment-polluted streams (Creed, 1994; Albertson and
Daniels, 2016). Beavers create habitats that facilitate inverte-
brates and amphibians, increasing density and biomass of
some species (Hood and Larson, 2014; Anderson et al., 2015).
Structure building invertebrates such as net-spinning caddis-
flies facilitate other benthic macroinvertebrates by providing
novel areas of refuge from fast water velocity (Cardinale
et al., 2001; Tumolo et al., 2019). However, a formal, quanti-
tative evaluation of the types and magnitude of positive inter-
actions is still lacking. As such, there are still many unknown
aspects of these important biotic interactions particularly in
freshwater ecosystems (Holomuzki et al., 2010; Silknetter
et al., 2020).
© 2020 John Wiley & Sons Ltd
Review And Synthesis
Figure 1 Number of publications in the data set
documenting a freshwater positive interaction by year
with a LOESS smoothing fit line. Dashed vertical
lines at 1994 and 2003 indicate years when influential
positive interactions papers were published (Bertness
and Callaway, 1994; Bruno et al., 2003).
Uncovering patterns of positive interactions in freshwaters
could be particularly useful for shedding light on general pat-
terns of biotic interaction related to stress and environmental
change. Specifically, the stress gradient hypothesis predicts that
positive interactions will be relatively stronger in environments
with larger environmental stress or consumer pressure (Peck-
arsky, 1983; Peckarsky et al., 1990; Zanetell and Peckarsky,
1996; Bertness and Leonard, 1997; Moore, 2006). The stress gra-
dient hypothesis has garnered mixed support, and almost
entirely from examination within terrestrial and marine ecosys-
tems (Callaway et al., 2002; Lortie and Callaway, 2006; Maestre
et al., 2006; Holmgren and Scheffer, 2010; Michalet et al., 2014).
In extreme cases, the positive outcome may be overwhelmed by
stressful physical conditions to the point when biotic interactions
are minimally relevant. Like terrestrial and marine ecosystems,
freshwater ecosystems are also stressful and show large daily and
seasonal variations in natural hydrologic properties, water tem-
peratures and sediment transport regimes (Resh et al., 1988;
Lytle and Poff, 2004; Magoulick, 2014). As such, they represent
ideal ecosystems with which to explore this important ecological
concept. Additionally, freshwaters are experiencing significant
increases in anthropogenic-driven stressors (Carpenter et al.,
1998; Strayer, 2010; Strayer and Dudgeon, 2010; Jenny et al.,
2020). These stressors include, but are not limited to pollution,
altered hydrology and species invasion, providing an opportu-
nity to consider how the type of stressor might mediate the
importance of positive interactions (Silliman and He, 2018). Yet
the stress gradient hypothesis’s application to freshwater ecosys-
tems remains largely untested and underrepresented (but see
Luo et al., 2010; Fugere et al., 2012; Peoples et al., 2015). The
evaluation of freshwater positive interactions is thus necessary
for continued and improved broad understanding of this foun-
dational ecological concept.
Review And Synthesis
Here we used meta-analysis to test the overarching hypothe-
ses that freshwater positive interactions are variable in magni-
tude across facilitator or beneficiary taxon, freshwater habitat
type, mechanism of benefit, facultative or obligate nature of
the relationship and invasive species status. We also tested
whether experiments that manipulated positive interactions in
the presence of a stress gradient showed stronger positive
interactions in a more stressful treatment. These comparisons
were motivated by classical work highlighting variation that
results from species identity, invasion status, type of facilita-
tion and stress (Jones et al., 1994; Callaway et al., 2002;
Strayer, 2010), as well as a recent review describing positive
interactions in freshwater ecosystems (Silknetter et al., 2020).
Response variables in our study ranged from the individual to
ecosystem level, including growth, reproduction, density, bio-
diversity and primary production. We quantitatively evaluated
106 peer-reviewed publications from across the globe that
investigated many different groups of organisms that partici-
pate in biotic interactions that are positive for at least one of
the participants (Figs 1 and 2). Our analysis provides synthe-
sised information regarding patterns of positive interactions in
freshwaters and identifies current knowledge gaps and future
research needs.
METHODS
Study selection
We performed a systematic search of the literature for studies
that documented a positive response on a beneficiary in the
presence of a facilitator in freshwater ecosystems. We con-
ducted the search using the online database Web of Science
Core Collection for articles containing the topics ((“aquatic”
OR “stream$” OR “river$” OR “freshwater$” OR “wetland$”
OR “lake$” OR “pond$” OR “vernal”) AND (“positive inter-
act*” OR “mutualis*” OR “commensal*” OR “facilitation”
OR “symbios*” OR “habitat ameliorat*” OR “stress amelio-
rat*” OR “ecosystem engineer*” OR “stress gradient*”) NOT
“blood stream”). The wildcards ($, *) represent unknown
characters and allow the search to capture articles containing
alternative forms of words. This search was further refined in
Figure 2 World map showing individual study
locations, number of studies per country and
examples of freshwater facilitator species commonly
studied in particular countries. Studied species from
left to right include the following: Zebra mussels,
beavers, golden mussels, common reed, California
blackworm and pondweed.
Freshwater positive interactions 3
Web of Science by only including articles in the categories in
Appendix 1. The search was conducted on February 3, 2020,
for all years available in the Web of Science Core Collection
(1900–2020). In addition to the systematic search, we
extracted all publications from a recent review of positive
interactions in freshwater (Silknetter et al., 2020) and a read-
ing list of publications compiled in 2018 by a local working
group on freshwater positive interactions. In total, our initial
search resulted in 2,943 publications. We further refined this
count by reading publication titles, abstracts or full text to
assess whether they met our inclusion criteria (see below),
which resulted in 106 publications with extractable data.
We developed a systematic protocol to decide whether pub-
lications would be included in our analysis, as well as proto-
cols to decide whether to include multiple data points in cases
when a single publication presented multiple studies docu-
menting a positive interaction (Nakagawa et al., 2017). To be
included, the study had to document a positive interaction in
a natural freshwater ecosystem, and at least one of the species
in the interaction had to be an obligate freshwater species.
For example a positive interaction between a fish and a terres-
trial plant was included, whereas an interaction between two
riparian plants was excluded, and a study occurring in an
agricultural holding pond or flooded agricultural field was
excluded. The study must have quantified a measurable
response or consequence of the positive interaction. For
example we did not include studies that simply described the
presence of a symbiosis between two species. We included
studies that obtained results from experimental or observa-
tional methods but excluded studies with results only from
simulation modelling. To be included, the methodological
approach must have had, at minimum, two treatments, one
with the facilitator (treatment group) and one without the
facilitator (control group). If these conditions were met, stud-
ies were included if we could extract an estimate for the mean,
sample size and uncertainty around the mean for both groups.
The facilitator must have had positive effects on the benefi-
ciary for the study to be included. If a study seeking positive
effects found neutral or negative effects, those data were not
included. Because we only included positive outcomes, our
data set is biased towards positive effect size values. This
© 2020 John Wiley & Sons Ltd
4 L. K. Albertson et al.
approach was necessary to address our questions regarding
patterns of positive interactions when they occur (see funnel
plot in Appendix 1, Figure S1). Untransformed data values
must have been reported to be included. And finally, when
the authors reported a positive interaction at multiple time
points, we extracted the value for the last time point when the
positive interaction occurred (Higgins and Green, 2011).
Data collection
From each publication, we extracted individual studies by
collecting means, standard errors and sample sizes for treat-
ment and control groups when a beneficiary responded pos-
itively to a facilitator. The presence or absence of a
facilitator could occur by experimental manipulation with
enclosures or exclosures, or through natural studies where
the facilitator was not present at the sampling site. Addi-
tionally, we extracted descriptive co-variates to describe
when, were and how positive interactions are studied in
freshwater. These co-variates included the (1) the geographi-
cal location of the study, (2) the response variable measured
in the study, (3) the invasion status of the facilitator (inva-
sive, non-invasive) as defined by the paper’s authors, (4) the
mechanism behind the positive interaction (habitat modifica-
tion, resource modification, cleaning symbiosis, etc.), (5) the
freshwater ecosystem (river, lake, vernal pool, etc.), (6) the
methodological approach of the study (field, mesocosm, lab-
oratory study), (7) the nature of the relationship between
facilitator and beneficiary (obligate, facultative) and (8) type
of interaction (direct, indirect, both). We extracted estimates
for means, uncertainty and sample sizes directly when pre-
sented in the main text or tables. If data were presented in
a figure, we used the imaging processing program ImageJ
along with the Figure Calibration plugin to extract mean
and uncertainty estimates (Schindelin et al., 2012). When
uncertainty estimates were presented using a metric other
than the standard error, we transformed the estimate to a
standard error using equations in Appendix 2. All publica-
tions from which data were extracted and used for analysis
can be found in Appendix 3.
Data analysis
We calculated log-response ratios (lnRR) for each study as
the standardised effect size for our meta-analysis (Hedges
et al., 1999). We chose this effect size because it is unitless,
and thus allows for comparisons across the broad range of
species, response variables and units used in the studies we
analysed. We calculated lnRR for each study using:

 
XT
lnRR ¼ ln  :
XC
The lnRR ultimately quantifies the log proportional change
between the treatment and control group (Lajeunesse, 2011).
In some studies, experiments compared multiple treatments
with a shared control group (e.g. the effect of a facilitator
taxon on a beneficiary with two treatments varying in benefi-
ciary density), which violates the assumption of independent
effect sizes for our models (Nakagawa et al., 2017). In these
© 2020 John Wiley & Sons Ltd
Review And Synthesis
cases, we pooled the treatment groups to derive a single-
weighted estimate for the mean as:
n1 T1 þ n2 T2
Xpooled ¼
n1 þ n2
where T1 and T2 are the mean effect sizes for the first and sec-
ond treatment, respectively, and n1 and n2 are the sample
sizes, and SD as:
vffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
 
u
uðnT  1Þσ2 þ ðnT  1Þσ2 þ nT1 nT2 X2 þ X2  2XT XT
t 1 T1 2 T2 nT1 þnT2 T1 T2 1 2
SDpooled ¼
nT1 þ nT2  1
where σ T1 and σ T2 are the standard deviations for the first
and second treatments. If more than two treatments shared a
control we applied this equation sequentially (treatments 1
and 2 first, then treatment 3, etc.; Higgins and Green, 2011).
While this method results in a slight loss of information and
statistical power, we felt it was appropriate considering the
variables we averaged across were not part of our research
questions, thus we retained the pertinent information of a
facilitator being present (Cheung, 2005; Scammacca et al.,
2014). We then calculated the within-study pooled variance
which was used to weight individual studies to minimise the
influence of studies with low statistical power during the anal-
ysis (Hedges and Olkin, 1985). We calculated the within-study
pooled sampling variance derived by Hedges et al., 1999 as:
 2  2
σ σ
varðlnRRÞ ¼ T 2 þ C 2

nT X nC X T C
We modelled patterns of positive interactions using a three-
level meta-analytic model using the ‘rma.mv’ function from
the R package metaphor (Viechtbauer, 2010). The three-level
model accounts for non-independence at both the publication
level (RefID in our data set), as well as the manipulation level
within a study as an individual publication could have multi-
ple manipulative treatments (Konstantopoulos, 2011). This
model structure allows for heterogeneity in the true effect sizes
between publications, as well as between experimental manip-
ulations within publications by adding a random intercept at
both levels of the hierarchy. We nested an experimental
manipulation inside RefID to account for publications that
reported multiple effect sizes and multiple manipulations using
the syntax (c. 1 | RefID / Manipulation). We fit separate mod-
els to investigate how the positive interaction varied across
each of the following moderator variables: facilitator type,
beneficiary type, facilitator invasion status, response variable,
facilitation mechanism, ecosystem and study methodological
approach. Effect size estimates were weighted by the inverse
of the marginal variance covariance matrix estimated by that
model (Viechtbauer, 2010).
We also analysed whether the effect of a positive interaction
on a beneficiary varied across a stress gradient to evaluate
support for the stress gradient hypothesis. The data set
included 13 studies that experimentally manipulated stress and
measured a beneficiary response. Each study paired a benefi-
ciary response at a low-stress level with a response at a high-
stress level. When a publication reported data from a study or
studies that manipulated more than two stress levels, we anal-
ysed only the highest and lowest stress values by coding the
Review And Synthesis
stress level variable as ‘H’ or ‘L’ respectively. Because we
drew multiple studies from the same publication, we modelled
the influence of stress on the response of a beneficiary species
using an identical nesting structure to account for non-inde-
pendence of effect size estimates and weighting as presented
previously.
We first fit models with an intercept term to obtain the
overall omnibus test, which indicates whether part of the
heterogeneity in the true effect size is related to some of the
moderators in the model. If the overall omnibus test for a
model indicated there were differences in the effect sizes
between the moderator variable groups (at α = 0.05), we refit
the model without an intercept term to test for differences
between the moderator variable levels. We used the ‘glht’
function from the R package multcomp (Hothorn et al., 2008)
to conduct all post hoc tests with a significance level of
α = 0.05, after a Bonferroni p-value adjustment to account
for the family wise error rate when conducting multiple com-
parisons. We report selected pairwise comparisons in the
results, however all pairwise comparisons can be found in
Appendix 4. We displayed effect size estimates of the lnRR in
figures, but we back-transformed response-ratios to present
the in-text results, which represent the percentage change in a
response with a facilitator present compared to a response
with no facilitator present. We used this back transformation
to aid in the interpretation of our modelled lnRR effect sizes
(Pustejovsky, 2018). All analyses were conducted using the R
Statistical Computing Environment, version 4.0.0 (R Core
Team 2020).
RESULTS
We found that freshwater positive interaction papers have
been published consistently since the mid 1980s but increased
in the early 1990s following on the heels of seminal papers,
with the largest increase in publication rate around the year
2000 (Fig. 1). Research occurred in 26 Countries, ranging
from 117 studies occurring in the United States to one study
occurring in both Panama and Spain (Fig. 2). For the 26
countries where studies occurred, the per capita study count
was, on average, 13.1 studies country-1. While 65 studies
occurred in Hungary, these were extracted from one publica-
tion that reported effect sizes for multiple taxa across four dif-
ferent facilitator groups (Bodis et al., 2014). Examples of
facilitators studied across the globe included beavers (Castor
sp.), zebra mussels (Dreissena polymorpha), golden mussels
(Limnoperna fortune), common reed (Phragmites australis),
pondweed (Potamogeton malaianus) and California blackworm
(Lumbriculus variegatus). Notably, no studies occurred in
Africa, Southeast Asia, the Middle East or Siberia.
We found that studies investigated a wide range of taxo-
nomic groups as the facilitator or beneficiary in a positive
interaction and facilitators were both invasive and non-inva-
sive (Fig. 3a and g). The most commonly studied freshwater
facilitators were mollusks and plants with 143 studies and 55
studies respectively. The least commonly studied freshwater
facilitators were periphyton and fungus with one study each.
For beneficiaries of positive interactions, we found that insects
and plants were the most studied occurring in 119 and 66
Freshwater positive interactions 5
studies respectively. The least commonly studied beneficiaries
were fungus and birds, with only two and one studies involv-
ing these groups respectively. In 73% of the studies, the facili-
tator was a non-invasive species (248 out of 340).
Studies quantified positive interactions by investigating
many different response variables, mechanisms, freshwater
ecosystems and methodological approaches (Fig. 3c, e, f and
h). We found that density was the most common response
variable used to quantify a positive interaction, which was
used in 34% of studies. Biomass and diversity were measured
less frequently, but still made up a substantial proportion of
the data set at 16% and 11% respectively. The least common
response variables measured were population growth (1.7% of
studies) and boldness (0.6%). Habitat modifications were the
dominant mechanism for positive interactions studied at 70%,
followed by resource modifications (26%). Cleaning symbioses
were studied least frequently as a mechanism and made up
just 1.2% of studies. Studies occurred in river and lake ecosys-
tems 89% of the time; however, we found that positive inter-
actions have also been documented in wetlands, carnivorous
plants, vernal pools and tree holes. Field studies were most
frequently used to investigate positive interactions (55%), fol-
lowed by mesocosm experiments (26%) and laboratory experi-
ments (19%).
Positive interactions also varied in the nature of the rela-
tionship between the facilitator and beneficiary and type of
interaction (Fig. 3b and d). An overwhelming majority of
studies (99%) involved facultative relationships between the
facilitator and beneficiary rather than an obligate relationship.
The three studies investigating obligate relationships involved
a cleaning symbiosis between a crayfish and an annelid worm.
Direct positive interactions were most common (227 studies),
followed by indirect interactions (73 studies), and a combina-
tion of both direct and indirect (40 studies).
We found minimal evidence that the facilitator group influ-
enced the strength of a positive interaction, and the omnibus
test was not significant (QM12 = 20.73, P = 0.06; Fig. 4a).
However, the effect size for a positive interaction depended
on the beneficiary group and the facilitator species’ invasion
status (Fig. 4b and c; see Appendix 3 for all pairwise compar-
isons). The strength of a positive interaction was stronger for
some beneficiary taxonomic groups compared to others
(QM12 = 38.78, P = 0.0001; Table S2). Across all responses
measured, mollusks experienced a 36.87% greater positive
response compared to insects (95% CI [9.77%, 55.83%]), but
no other beneficiary taxonomic groups differed in their posi-
tive response. The strength of positive interactions also varied
based on the invasion status of the facilitator species (QM1 =
8.69, P = 0.0032; Table S3). The strength of a positive inter-
action was 25.85% smaller when a non-invasive group was
the facilitator compared to an invasive group (95% CI
[−39.22%, −9.54%]).
The strength of a positive interaction also differed based on
the response variable measured (QM11 = 194.93, P < 0.0001;
Fig. 4D; Table S4). Compared to the two most frequently
used response variables (density, biomass), we found little evi-
dence that positive interactions influenced diversity, which
only increased by an estimated 10.86% (P = 0.1657). Compar-
atively, a density response was 85.92% stronger (95% CI
© 2020 John Wiley & Sons Ltd
6 L. K. Albertson et al. Review And Synthesis

Figure 3 Lollipop plots displaying the number of studies across moderator variables. (a) Facilitator and beneficiary taxonomic groups; (b) Interaction type;
(c) Freshwater ecosystem where positive interaction occurred; (d) Nature of the species’ relationship; (e) Response variable used to measure a positive
interaction; (f) Mechanism supporting the positive interaction; (g) Invasion status of the facilitator and (h) Study methodological approach used to
investigate positive interactions.

[54.02%, 116.44%]) and a biomass response was 98.67%
stronger (95% CI [57.53%, 150.56%]) than a diversity
response. Positive interaction magnitudes also varied based on
the mechanism underpinning the interaction (QM3 = 8.80,
P = 0.0320; Fig. 4E; Table S5), as well as the study method-
ological approach (QM2 = 11.59, P = 0.0030; Fig. 4G). Habi-
tat modifications were associated with a 33.67% greater
positive effect than those associated with a resource modifica-
tion (95% CI [3.85%, 72.05%]). No differences across ecosys-
tem types were detected (Fig. 4f; Table S6). Effect sizes for
positive interactions measured in the field were 44.06% stron-
ger than those measured in a laboratory environment (95%
CI [10.08%, 88.52%]). Mesocosm studies were not different
than field studies or laboratory studies (Table S7), and inter-
action strengths did not vary based on the type of interaction
(Fig. 4h; Table S9) or the nature of the relationship between
facilitator and beneficiary (Fig. 4i; Table S8).
We found no evidence that positive interaction strengths are
modified by stress (QM1 = 0.66, P = 0.4169; Fig. 5). In this
subset of studies, consumer pressure and nutrients were the
stressors evaluated (Fig. 5). Compared to a control without
the facilitator, a positive response was 98% greater in the
presence of a facilitator in high-stress conditions (P = 0.0902)
and 118% greater in a low-stress condition (P = 0.0516), but
high and low-stress levels did not differ from one another.
DISCUSSION
Positive interactions are important in natural ecosystems; how-
ever, we know far less about their prevalence, magnitude and
responses to invasive species and stressors in freshwater ecosys-
tems compared to others. Our data set was comprised of positive
interaction papers that have been published consistently since
the 1980s. We observed a gradual increase in paper numbers

© 2020 John Wiley & Sons Ltd

Review And Synthesis Freshwater positive interactions 7

Figure 4 lnRR effect sizes for positive interaction strengths across moderator variables. (a) Facilitator taxonomic groups; (b) Beneficiary taxonomic groups;
(c) Invasion status of the facilitator; (d) Response variable used to measure a positive interaction; (e) Mechanism supporting the positive interaction; (f)
Freshwater ecosystem where positive interaction occurred; (g) Study methodological approach; (h) Interaction type and (i) Nature of species’ relationship.
P-value for the overall omnibus test is shown in the bottom right corner of each panel. Error bars are 95% confidence intervals. Red dashed line at
lnRR = 0 shows location of no effect.

through the mid-1990s, with the largest rate of increase in the
early 2000s, a timeline that aligns well with the publication of
several seminal research papers and reviews highlighting the
need for but understudied value of positive interactions in ecol-
ogy (Bertness and Callaway, 1994; Jones et al., 1994; Stachowicz,
2001; Bruno et al., 2003). Rivers and lakes comprised the vast
majority of habitats studied in our data set, but no significant dif-
ferences were detected in the strength of positive interactions
across any habitats, suggesting these biotic interactions are ubiq-
uitously important. Freshwater positive interactions influenced
beneficiaries in many ways, including increasing density, coloni-
sation rates, reproduction and survival. However, positive inter-
actions had relatively small impacts on biodiversity, population
growth and boldness. Non-invasive facilitators were more com-
monly studied, but invasive facilitators had significantly stronger
positive effects. Mollusks benefited significantly more than
invertebrates. Amphibian and biofilm beneficiaries showed the
largest magnitude positive responses, but these were not different
from one another or from other groups. These findings suggest
positive interactions are taxon-specific, but prevalent across
kingdoms. It was encouraging to see that field studies showed
significant positive responses overall, suggesting that freshwater
ecologists are successfully detecting and quantifying positive
interactions in natural settings. We found no support for stron-
ger effects of positive interactions in high stress treatments in the
few experiments that have tested a beneficiary response to the
presence of a facilitator at various stressor levels. Our findings
contribute a quantitative evaluation of the scope of positive
interactions in freshwater ecosystems and generally concur with
a recent review highlighting positive interaction research across
different freshwater facilitator and beneficiary taxa (Silknetter
et al., 2020).

© 2020 John Wiley & Sons Ltd

8 L. K. Albertson et al.
Figure 5 Weighted lnRR effect sizes and 95% confidence intervals for 13 studies that recorded a positive response in the presence of a facilitator in both
high (dark blue) and low stress (light blue) conditions. Effect sizes are weighted by the inverse of the marginal variance covariance matrix estimated by the
model and displayed by varying the size of the estimated mean lnRR point. Group means plotted as diamonds with width of diamond representing 95%
confidence interval. Red dashed line at lnRR = 0 shows location of no effect.
Our data set identified a total of 14 studied taxonomic
groups as either facilitators or beneficiaries across a range of
trophic positions and evolutionary histories. Mollusks were by
far the most commonly studied facilitators. Their sensitivity
to anthropogenic change and status as prolific invaders per-
haps has driven the extensive interest in this particular group
(Ram et al., 1992; Lydeard et al., 2004; Duchini et al., 2018).
Mollusks often facilitate submerged macrophytes by reducing
algal blooms that might otherwise hinder macrophyte growth
by limiting light availability (He et al., 2014). They also facili-
tate macroinvertebrates by providing predator refugia and
increasing survival (Kobak et al., 2014). Other common facili-
tators were plants and insects. Plants and aquatic insects mod-
ify freshwater physical processes such as erosion and sediment
deposition in ways that create unique habitats or alter
resource availability for beneficiaries (Dodds, 1991; Fritz
et al., 2004; Reinhardt et al., 2010; Albertson and Allen,
2015). Periphyton had the strongest facilitative effect but was
studied much less frequently than crustaceans, fish, insects,
plants and mollusks and the strong effect was demonstrated
by a single study (Medina-Sanchez et al., 2004), highlighting
the need to further investigate this group’s status as a facilita-
tor.
© 2020 John Wiley & Sons Ltd
Review And Synthesis
Aquatic insects were the most studied beneficiary, a finding
that is supported by decades of research using this particular
group to investigate general patterns of disturbance, feeding
relationships, organic matter processing and biomonitoring in
freshwater ecosystems (Karr, 1991; Wallace and Webster,
1996; Covich et al., 1999). For example mayflies respond posi-
tively to habitat and predator refuge provided by mussels in
soft-sediment, lentic ecosystems (DeVanna et al., 2011). Lam-
preys building nests alter physical substrate conditions and
thereby increase density of benthic invertebrates (Hogg et al.,
2014). Mollusks were also commonly studied as beneficiaries.
Production, colonisation and reproduction of beneficiaries all
showed the largest magnitude effects but were not studied as
frequently as other response variables such as density and bio-
mass, suggesting there is room to understand these responses
further. Although many studies show that positive interactions
enhance biodiversity (Hacker and Gaines, 1997; Mulder et al.,
2001), our findings revealed that the magnitude of positive
interactions on diversity in freshwater is small. Perhaps posi-
tive interactions in freshwater are realised more commonly
through pairwise interactions specifically, and as such, no or
little effect on diversity per se is to be expected. That is, some
species benefit while others do not, resulting in minimal
impacts on community diversity as a whole, a topic that has
Review And Synthesis
received attention in marine and terrestrial ecosystems but
needs additional evaluation in freshwaters given our findings
(Hoeksema and Bruna, 2000; Stanton, 2003). Alternatively,
research on freshwater positive interactions may be at a stage
in which researchers have yet to utilise or develop accurate
approaches for measuring community-level responses for
detecting relationships between positive interactions and bio-
diversity (Silknetter et al., 2020).
The mechanism of positive interaction influenced how
strongly the positive benefit was conferred, and habitat modi-
fication more strongly benefited participants than resource
modification did. In freshwater research, ecosystem engineer-
ing terminology has been utilised extensively to emphasise the
strong links between organisms and physical habitat modifica-
tion (Moore, 2006; Jones, 2012; Atkinson et al., 2018). This
link was strongly supported by our finding that habitat modi-
fication was identified by researchers as the mechanism of
positive interaction almost four times as often as resource
modification. However, many studies suggested that both
habitat modification and resource modification were occur-
ring. In several cases, positive interactions were experienced
when one predator increased prey amount or ease of capture
for another predator (Soluk and Richardson, 1997; Kelly
et al., 2002). Along with habitat and resource modifications,
cleaning symbioses are important mechanisms of freshwater
positive interactions. Cleaning symbioses highlight the con-
text-dependency of positive interactions. Crayfish, for example
have worms that benefit from eating parasites off of their gill
structures, with certain crayfish species or life-stages benefiting
more than others (Thomas et al., 2016). The magnitude of
positive outcomes from cleaning symbioses was small overall,
and future work might evaluate how they compare to well-
recognised cleaning relationships in marine systems (Brown
et al., 2002; Schemske et al., 2009). Overall, a variety of mech-
anisms were studied, but habitat modification was the most
common and strongest positive interaction.
Invasive facilitators had a stronger positive influence than
non-invasive facilitators. Perhaps, invasive facilitators occur in
high densities, have traits that lead to disproportionately large
positive effects, or play a strong role in already-degraded,
stressed ecosystems where beneficiaries have more opportunity
to respond positively (MacDougall and Turkington, 2005;
Ramus et al., 2017). A more explicit identification of invasive
facilitator traits may inform species distribution models that
account for positive biotic interactions (Maestre et al., 2009;
Kissling et al., 2012; Tikhonov et al., 2017; Wagner et al.,
2020). These traits may be particularly tied to habitat modifi-
cation, the mechanism showing the strongest positive response
in our data set (Crooks, 2002). Although a large portion of
research on invasive species highlights their negative impacts
(Vitousek et al., 1997; Strayer, 2010; Rogosch and Olden,
2020), the role of invasive species is complex, resulting in
simultaneous positive and negative influences when some spe-
cies benefit but others do not (Rodriguez, 2006; Collins et al.,
2017). For example invasive zebra mussels positively influence
benthic primary producers by filtering water and improving
clarity and their shells provide novel habitat to mayflies,
whose populations increase in abundance (Cecala et al., 2008;
DeVanna et al., 2011). Because invasive facilitators do show
Freshwater positive interactions 9
substantial positive benefits to some species, it may be difficult
for managers to evaluate how and when to remove invasive
species if they confer positive effects for some but not all taxa.
Invasive species that have positive effects that increase a bene-
ficiary may also not ultimately equate to desirable ecological
outcomes when they increase the abundance or biomass of
beneficiaries beyond natural levels, drastically alter food web
dynamics and nutrient cycling, or even cause invasional melt-
down, when synergistic interactions among invaders lead to
accelerated impacts on native ecosystems (Simberloff and Von
Holle, 1999; Hall et al., 2006; Braga et al., 2018). Thus,
understanding the role and management of invasive facilita-
tors poses an important contemporary ecological challenge.
Despite numerous tests of the stress gradient hypothesis in
terrestrial and marine systems (He et al., 2013), we found only
a small number of quantitative experimental tests related to
stress and positive interactions in freshwaters. Our data set
included 13 studies that manipulated stress in an experimental
setting, and these studies showed, on average, no difference in
positive interaction effect size between high- and low-stress
treatments. Many of these studies did not explicitly aim to test
the stress gradient hypothesis, which predicts that the fre-
quency or relative importance of positive interactions increase
with stress (Peckarsky et al., 1990; Bertness and Callaway,
1994). Instead, studies in our data set investigated the magni-
tude or strength of positive effect in high stress compared to
low-stress treatments (Bruno et al., 2003). Given that we did
not evaluate whether the frequency of positive interactions
increases as stress increases, our findings do not exhaustively
indicate that the stress gradient hypothesis is not supported in
freshwater ecosystems. Rather, they highlight the need for
much more work on this topic and the potential for future
studies to evaluate outcomes when various stressors or various
responses of positive effects are measured (He et al., 2013).
For example, multiple stressors are common in freshwater
ecosystems (Heugens et al., 2001; Ormerod et al., 2010) and
can show antagonistic rather than synergistic influence. Per-
haps, this outcome dampens the positive influence of facilita-
tors under stressful conditions. Furthermore, two types of
stressors included in the original stress gradient hypothesis,
consumer pressure and physical stress, more often than not
vary directly and not inversely, suggesting that coupled stres-
ses will increase at a faster rate and the importance of positive
interactions will be further pertinent (Silliman and He, 2018).
Stress can be realised as both natural variation in abiotic con-
ditions such as flow or predatory conditions such as high den-
sities of enemies, as well as anthropogenic variation caused by
damming, pollution and others (Silknetter et al., 2020). Defin-
ing how stress is experienced by beneficiaries, as well as the
thresholds where facilitation alleviates stress, has been a major
criticism and challenge for the stress gradient hypothesis
(Maestre et al., 2009; He and Bertness, 2014). Given the
increasing degradation of water quantity and quality stem-
ming from anthropogenic stressors, this topic deserves sub-
stantially further exploration (Vörösmarty et al., 2010; Bunn,
2016). Human activities are amplifying the number and mag-
nitude of stressors in natural ecosystems, making it increas-
ingly important to be able to define stress across
environmental context and understand biotic interactions in
© 2020 John Wiley & Sons Ltd
10 L. K. Albertson et al.
the face of global change (Hammarlund and Harcombe, 2019;
Piccardi et al., 2019).
Although an increase in the number of studies investigating
positive interactions in freshwater jumped through the 1990s,
perhaps aligning with a more general trend in ecology on the
heels of high-profile papers, there are still several important
areas for future research. Our literature search resulted in an
extensive 2,943 papers on the topic of positive interactions in
freshwater ecosystems, but relatively few of these papers ulti-
mately met the quantitative criteria of reporting a mean, error
and sample size required to be included in the meta-analysis,
highlighting the need for researchers to more thoroughly
report their experimental designs and results. A recent review
by Silknetter et al. (2020) outlined areas for future research in
freshwater positive interactions, and the findings from our
data compilation align with these directives. For example, rel-
atively few studies conducted work that measured responses
over space or time. Limited spatial and temporal measure-
ments suggest that ecologists still cannot address important
questions of positive interactions in ecology because we are
not reporting work across scales (Jablonski, 2008; McGill,
2010). Negative interactions have seen important progress in
this area (McLaughlin and Roughgarden, 1992; Fausch, 1998;
Chizzola et al., 2018; Weiss, 2019), but this topic will be an
important future step for freshwaters, especially as spatial and
temporal variation relates to stress gradients (He et al., 2013;
Tumolo et al., 2020). Effects of facilitators on populations
and communities is another important topic for future
research. A species niche may be expanded by positive interac-
tions, but how these relationships vary across time or space
remains an active area of research (Chase and Myers, 2011;
Bulleri et al., 2016). Whether positive interactions maintain
rare species in freshwater communities has not yet been inves-
tigated (Calatayud et al., 2020), but our findings suggest that
sensitive and increasingly rare but important groups such as
amphibians, fish and mollusks can benefit substantially from
positive interactions (Pintor and Soluk, 2006; Whiles et al.,
2006; Peoples et al., 2011). The vast majority of positive inter-
actions included in our data set were direct interactions, but
indirect or some combination of the two interactions had just
as large of an influence on beneficiaries, perhaps suggesting
that indirect positive interaction cascades that influence com-
munity-level metrics such as biodiversity are a possible new
frontier in freshwater science (Thomsen et al., 2010). And
finally, the relative importance of positive interactions com-
pared to negative interactions has not yet been established for
freshwater ecosystems. Although several reviews have high-
lighted progress in our understanding of biotic interactions,
the relative importance of both negative and positive interac-
tions and especially their context-dependency has yet to be
identified (Thorp, 1986; Soluk and Collins, 1988; Mermillod-
Blondin and Rosenberg, 2006; Holomuzki et al., 2010; Correa
et al., 2015b). This topic has provided some important
insights in terrestrial and marine ecosystems (Bertness et al.,
1999; Stewart et al., 1999; Hay et al., 2004; Duchini et al.,
2018; Prugh and Sivy, 2020). As such, an evaluation of the
relative magnitude of positive interactions in freshwater habi-
tats compared to negative interactions is an important next
step.
© 2020 John Wiley & Sons Ltd
Review And Synthesis
In conclusion, we used meta-analysis to elucidate patterns
of freshwater positive interactions and found that they are
widespread and participated in by many different taxonomic
groups. The similar strength of positive interaction across
freshwater habitats was surprising given the large variability
in physical constraints and organismal adaptations from those
different habitat types. Rare species or species of concern such
as amphibians and mollusks may be most susceptible to alter-
ation of positive interaction networks under global change
(Correa et al., 2015a). Critical areas for future research are to
further investigate the role of positive interactions compared
to negative interactions, the strength of positive interactions
in freshwater compared to terrestrial and marine, and to bet-
ter identify stressors and how they modify the strength of pos-
itive interactions. Our findings provide the first quantitative
synthesis of positive interactions in freshwaters, highlight the
ubiquity of freshwater positive interactions and identify
important research areas for future knowledge generation.
ACKNOWLEDGEMENTS
We thank L. Calle, W. Cross and E. Scholl for discussion and
constructive feedback during manuscript development. Three
reviewers provided comments that greatly improved the
manuscript. Funding was provided for LKA, MJM and BBT
in part by the National Science Foundation (DEB 1556684)
and Montana State University. Funding for MAB was pro-
vided in part by The National Park Service (P17AC01089).
AUTHORSHIP
LKA conceived the original idea; All authors designed the
research and collected the data; MJM analysed the data;
LKA and MJM wrote the original paper draft; All authors
contributed substantially to revisions.
PEER REVIEW
The peer review history for this article is available at https://
publons.com/publon/10.1111/ele.13664.
DATA AVAILABILITY STATEMENT
The data supporting the results are archived in Dryad
(https://doi.org/10.5061/dryad.zcrjdfn9b).
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