# Control mechanisms of photosynthetic epibionts on zooplankton: an experimental approach

Andrea Bertolo, Marco A. Rodriguez, Gérard Lacroix

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Andrea Bertolo, Marco A. Rodriguez, Gérard Lacroix. Control mechanisms of photosynthetic epibionts on zooplankton: an experimental approach. Ecosphere, 2015, 6 (11), 10.1890/ES14-00451.1. hal-02634868

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# Control mechanisms of photosynthetic epibionts on zooplankton: an experimental approach

ANDREA BERTOLO,<fnref n="1" />,† MARCO A. RODRÍGUEZ,<fnref n="1" /> AND GÉRARD LACROIX<fnref n="2" />,<fnref n="3" />

**Citation:** Bertolo, A., M. A. Rodríguez, and G. Lacroix. 2015. Control mechanisms of photosynthetic epibionts on zooplankton: an experimental approach. Ecosphere 6(11):219. http://dx.doi.org/10.1890/ES14-00451.1

**Abstract.** Several top-down and bottom-up forces have been put forward to explain variable infestation rates of zooplankton by epibionts. Among top-down forces, fish predation affects epibiont prevalence on zooplanktonic organisms, either by eliminating more conspicuous, heavily burdened individuals, or by reducing population size of zooplankton hosts, with consequences for substrate availability for epibionts. However, detailed experimental-based information on the effects of top-down forces is still lacking. Among bottom-up forces, light can potentially control populations of photosynthetic epibionts. Therefore, both changes in light penetration in the water column and the vertical position of hosts in the water column could affect the photic conditions in which epibionts live and could thus control their population growth. We tested experimentally the hypothesis that both light limitation and fish predation affect epibiont burden on zooplankton. Moreover, we also tested the hypothesis that zooplanktivorous fish affect the prevalence and burden of the epibiotic alga *Colacium* sp. (Euglenida) on zooplankton not only by direct predation, but also by affecting the vertical distribution of zooplankton. We analyzed *Colacium* burden on two zooplankton genera that responded differently to the presence of zooplanktivorous fish by altering their daytime vertical distributions, thus exposing photosynthetic epibionts to different light conditions. *Colacium* burden on the two zooplankton genera was also compared between enclosures with different degrees of light limitation. Our results suggest that (1) ambient light limitation has the potential to reduce the burden of photosynthetic epibionts on zooplankton in natural conditions, and (2) zooplankton behavior (e.g., daytime refuge use to escape fish predation) can reduce the burden by exposing photosynthetic epibionts to suboptimal light conditions.

**Key words:** Bayesian framework; *Ceriodaphnia*; *Colacium*; *Diaphanosoma*; epibiosis; fish predation; light limitation; non-consumptive effects; shared doom hypothesis; zooplankton vertical distribution.

**Received** 19 November 2014; revised 4 March 2015; accepted 18 March 2015; published **12 November 2015**.
**Corresponding Editor:** E. García-Berthou.

**Copyright:** © 2015 Bertolo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. http://creativecommons.org/licenses/by/3.0/

† **E-mail:** andrea.bertolo@uqtr.ca

## INTRODUCTION

Epibiosis is a form of inter-specific interaction that is commonly found in aquatic ecosystems (e.g., Cattaneo and Kalff 1980, Bickel et al. 2012).

It could result in parasitism, mutualism or commensalism (e.g., Decaestecker et al. 2005) and could have important direct community-wide effects, such as the collapse of host populations due to shading (Sand-Jensen 1977).

<footnote n="1">¹Research Centre for Watershed, Aquatic Ecosystem Interactions and Département des Sciences de l'Environnement, Université du Québec à Trois-Rivières, C.P. 500, Trois-Rivières, Québec G9A 5H7 Canada</footnote>

<footnote n="2">²UMR 7618-iEES Paris (CNRS, UPMC, UPEC, Paris Diderot, IRD, INRA), Institute of Ecology and Environmental Sciences, Université Pierre et Marie Curie, Bâtiment A, 7 quai St Bernard, 75252 Paris cedex 05 France</footnote>

<footnote n="3">³UMS 3194 (CNRS, ENS), CEREEP, Ecotron IleDeFrance, Ecole Normale Supérieure, Station biologique de Foljuif, 78 rue du Château, 77140 St-Pierre-lès-Nemours, France</footnote>
Indirect population and community-wide effects are also possible because epibionts have the potential to alter the interactions between the host and its environment (Wahl 2008a, b). Epibionts can, for example, alter host vulnerability to predators which can, in turn, have an impact on food-web dynamics (Wahl et al. 1997, Wahl 2008a). Despite these potential effects, epibiosis has attracted relatively little interest in ecology and much of our knowledge on this form of parasitism still stems from case studies (e.g., Hanamura 2000, Regali-Seleghim and Godinho 2004). Moreover, although our knowledge of the effects of epibionts on hosts is expanding (e.g., Stirnadel and Ebert 1997, Barea-Arco et al. 2001), very little is known about the effects of hosts (e.g., in terms of abundance or behavior) on epibiont populations.

Zooplanktonic organisms are known to be used as substrates by an array of different epibiont taxa such as bacteria (Grossart et al. 2010, Tang et al. 2010), ciliates (Bickel et al. 2012) and euglenoids (Al-Dharheri and Willey 1996). Epibionts attached to zooplanktonic organisms have been shown to have great potential to affect the functioning of aquatic systems, for example, by controlling whole-lake bacterial respiration (Tang et al. 2010) or remineralization (Bickel et al. 2012).

Hosts are not inert substrate for epibionts. For example, molting in crustacean zooplankton drives a constant renewal of substrate that has both positive and negative effects for the epibionts. Although molting reduces competition for the substrate, during inter-molt phases the epibionts must become mobile and be therefore exposed to zooplankton grazing (Barea-Arco et al. 2001). Factors usually postulated to potentially benefit zooplankton epibionts include the use of zooplankton excretion products and increased dispersal due to hitchhiking on mobile zooplankton (Grossart et al. 2010). Whereas some positive effects of epibionts on host have been observed (Barea-Arco et al. 2001), most studies have focused on the costs of epibiont burden on zooplankton hosts (e.g., increased drag and reduction of fecundity) (Threlkeld and Willey 1993, Gilbert and Schroder 2003). Increased exposure to fish predation because of greater visibility is a potential cost for both host and epibionts (Willey et al. 1993). This latter phe-

nomenon (a “shared doom” effect, sensu Wahl 1997, 2008a), demonstrated to date only on epibiont prevalence (Willey et al. 1993), might be essentially an indirect effect of fish size-selectivity. Fish might in fact reduce epibiont prevalence simply by eliminating larger zooplankton, which are more likely to carry epibionts (Threlkeld and Willey 1993). It is therefore necessary to control for host body size to confirm that a shared doom effect exists in this kind of epibiosis. Non-consumptive effects of fish on host behavior, such as diel vertical migration, (Lampert 1989) could also expose epibiont organisms to sub-optimal conditions (Threlkeld et al. 1993). It is therefore necessary to take into account both consumptive and non-consumptive effects of predators to understand their overall impact on epibiont populations.

In this paper, we analyzed the interactive effects of predation and light limitation in determining the burden of *Colacium* sp. (Euglenophyceae), a photosynthetic epibiont, on *Ceriodaphnia* and *Diaphanosoma*, two cladoceran genera that show different responses to fish predation, both in terms of consumptive and non-consumptive effects (Bertolo et al. 1999b). Our aim is to analyze epibiosis in a trophic context and demonstrate experimentally that: (1) there is a shared doom effect in the presence of fish, i.e., that the negative effects of fish on epibiont burden is not only a by-product of fish size selectivity; (2) light limitation has the potential to reduce photosynthetic epibiont burden; and (3) non-consumptive effects on host behaviour have the potential to modulate light limitation for epibionts.

To reach these objectives, we used zooplankton samples from an in situ mesocosm experiment in which we already demonstrated that predation and light limitation have clear additive effects on lower trophic levels (Bertolo et al. 1999a). Moreover, we also showed that both consumptive and non-consumptive effects of fish differ between the two selected cladocerans (Bertolo et al. 1999a). More specifically, *Ceriodaphnia* responds more heavily to predation than *Diaphanosoma* in terms of reduction of individual size and total population biomass, and also in terms of daytime vertical distribution. Bertolo et al. (1999b) showed that only *Ceriodaphnia* shifted from a relatively homogeneous distribution in
the water column (either with or without fish), to a relatively huge concentration in the bottom layers if the deeper part of the water column was protected from the fish predators presents. As this system has been shown to be light-limited (Bertolo et al. 1999a), we expect to find lower epibiont burdens for a given host size when the hosts use deepwater (i.e., dark) refuges. This provides an ideal setup to analyze the non-consumptive effects of fish on epibiont burden.

The three main hypotheses were tested as follows: (1) the shared doom effect hypothesis was tested by comparing the *Colacium* burden (corrected for host body size) on the two host genera under different predation pressures; (2) the light limitation hypothesis was tested by comparing *Colacium* burden on host collected from enclosures of different depth, that differed in their level of light limitation; and (3) the non-consumptive effects hypothesis was tested by comparing *Colacium* burden in host that differ in their use of light-limited strata when exposed to fish predation. Here, controlling for the consumptive effects of fish was key to properly analyze their non-consumptive effects on epibiont burden, together with the effects of light limitation.

## METHODS

### Experimental design

The experiment was conducted in Lake Créteil (48°46′37″ N, 2°26′47″ E), a small (42 ha), shallow (mean depth: 4 m, maximum depth: 6 m) sand-pit lake situated 15 km SE of Paris, France. Fifteen experimental enclosures made of translucent polyethylene (300 µm thickness) were reached 25 cm above the lake surface, inside a rectangular pontoon. Each enclosure was open to the atmosphere and completely sealed at the bottom. Enclosures of two different sizes were used, with a constant wall area/volume ratio: deep enclosures (1.5 × 1.5, 4.5 m depth; volume 9.5 m³) and shallow ones (1.5 × 1.5, 2.5 m depth; volume 5 m³). We explicitly chose the shape of the enclosures to reduce differences in optical condition related to wall reflectance. It has been demonstrated that using enclosures with a constant cross-section should homogenize patterns of periphyton growth and help to reduce the bias tied to this wall artifact (Chen et al.

1997). The enclosures were filled with lake water, taken at 1.5 m depth with a gasoline-powered pump. In order to minimize seston heterogeneity, bags were filled randomly and in several steps between 29 June and 3 July 1995. Taking into account differences in enclosure size, we filled each day equal portions of total enclosure volume. Enclosures were thereafter enriched, proportionally to their volume, with living zooplankton netted in the pelagic zone of the lake. To allow for initial development of the planktonic community, fish enclosures were stocked with roach (*Rutilus rutilus*) only on 13 July (hereafter called day 0). At day 0, zooplankton biomass in enclosures was >200 mg DW L⁻¹. Five different treatments, each having three replicates, were randomly applied to the 15 enclosures (NF = no fish, F = fish, S = shallow, D = deep, R = refuge):

1. NFS: shallow enclosures without fish

2. FS: shallow enclosures with 6 fish; 20.6 g fresh weight FW m⁻²

3. NFD: deep enclosures without fish

4. FD: deep enclosures with 6 fish; 20.6 g FW m⁻²

5. FDR: similar to FD, but with fish confined in the surface layer (0–2 m) of the enclosure in a net-bag (1.5 × 1.5; 2 m depth; 23 mm² maximum mesh size) that allowed zooplankton passage.

Fish length measurements were taken to the nearest millimetre. To reduce manipulation of fish used for the treatments, the initial body mass of roach was estimated from a sample of fish of the same origin as those stocked in the enclosures. Average roach fork length (FL) was 8.1 ± 0.4 cm (mean ± SD) and fresh weight was 7.5 ± 0.4 g (mean ± SD). To avoid nutrient limitation of phytoplankton, enclosures were enriched with inorganic fertilizers. Because phytoplankton experience nutrient limitation on a volumetric basis (Petersen et al. 1997), we used volume to scale nutrient load. Nutrients were added twice a week as a liquid mixture of potassium phosphate (KH₂PO₄) and ammonium nitrate (NH₄NO₃) with an N:P ratio of 20:1 by weight, for a load of phosphorus equal to 3.16 µg L⁻¹ d⁻¹. Epibiont development was followed weekly during 21 days after day 0 by collecting vertically integrating
ed zooplankton samples. To analyze separately
epibiont burden on hosts having different posi-
tions in the water column (deep enclosures only),
on the second sampling occasion we separated
samples from surface (0–2 m) and bottom layers
(2–4 m). Zooplankton were counted under a
stereoscopic microscope in subsamples at differ-
ent dilutions in Dolfuss chambers (four to five
subsamples per sample). When individuals were
rare, the whole sample was analyzed. Crustacean
body length and epibiont burden were measured
with an ocular micrometer for 40 randomly
chosen individuals per taxon in each sample.
Epibiont burden was measured for each individ-
ual host on an ordinal 0–4 scale (0 = absence; 1 =
1–3 ind; 2 = 4–10 ind.; 3 = 11–50 ind.; 4 = more
than 50 ind). While losing precision relative to
full sample counts, this method allowed to
estimate epibiont burden on a large number of
hosts and in a relatively large number of
experimental units. Zooplankton biomass was
calculated by genus as in Bertolo et al. (1999a).
Four cladoceran genera were present in the
enclosures: *Ceriodaphnia*, *Bosmina*, *Diaphanosoma*,
and *Daphnia*. Three copepod genera were also
present: *Acanthocyclops*, *Thermocyclops* and *Eu-
diaptomus*. With the exclusion of *Bosmina*, all
cladocerans commonly hosted *Colacium* sp. with
a variable burden. *Daphnia* epibiont burden was
not analyzed here because this genus was rare in
the fish enclosures. Among copepods, only the
cyclopoid *Acanthocyclops* and the calanoid *Eu-
diaptomus* showed occasionally a light epibiont
burden. *Colacium* sp. was only observed on the
former, whereas the latter hosted an unidentified
stalked ciliate.

In addition to individual body length and
mass of hosts, we calculated total host biomass as
an index of potential sources of epibiont recolo-
nization. Total host biomass was calculated as the
sum of biomass over all the taxa observed to host
epibionts in our experimental enclosures (i.e.,
*Daphnia*, *Ceriodaphnia*, *Diaphanosoma*, and *Acan-
thocyclops*). Analyses were run with and without
*Acanthocyclops* in the pool of hosts because
overall epibiont prevalence was low for this
genus. Additional details on the experimental
setup and on zooplankton counts can be found in
Bertolo et al. (1999*a*, *b*).

Background information:

predation refuges and host vertical distribution

Experimental treatments had a clear impact on
the individual body size and abundance of both
host genera, with clear consequences on their
biomass (Table 1). Fish predation had a clear
negative effect on the body size of both genera,
whereas the presence of refuge somewhat re-
duced this effect (Table 1). Whereas *Diaphanoso-
ma* abundance and biomass were not strongly
affected by fish predation, *Ceriodaphnia* showed a
clear reduction of numbers in the presence of fish
(Table 1). However, the availability of physical
refuge (FDR) allowed *Ceriodaphnia* to maintain a
population biomass comparable to that of the
control (NFD) even in the presence of fish.

Previous analyses of the daily vertical distri-
bution of zooplankton in our experimental
enclosures showed that use of the water column
by *Ceriodaphnia* was clearly affected by the
presence of fish and of physical refuge (Bertolo
et al. 1999b). In the absence of fish (NFD
treatment), *Ceriodaphnia* was slightly more abun-
dant in the lower than in the upper enclosure,
whereas the opposite pattern held in the presence
of fish (Table 1). The presence of the refuge
dramatically changed the vertical distribution of
*Ceriodaphnia* in the presence of fish (FDR vs FD
treatment), with most individuals concentrating
during the day in the bottom, predator-free, layer
(Table 1). In contrast, *Diaphanosoma* vertical
distribution was rather homogeneous among
the treatments (Bertolo et al. 1999b), with
individuals slightly more abundant in the lower
(60–70% ca.) than in the surface layer (Table 1).

In absence of light limitation, we should expect
that *Ceriodaphnia* size-corrected epibiont burden
in the presence of the refuge would be interme-
diate between epibiont burden in fish and
fishless enclosures without refugia. In fact, both
mean *Ceriodaphnia* body size and total biomass
resulted to be intermediate relatively to fish
(without refugia) and fish enclosures in the
presence of deepwater refugia. However, since
the vertical distribution of *Ceriodaphnia* was
strongly affected by the presence of refugia, we
expect that epibiont burden would be strongly
reduced because of light limitation, once con-
trolled for host size. We expect to find no
difference in *Diaphanosoma* epibiont burden
between fish enclosures (with or without refugia)
<table><caption>Table 1. Abundance, biomass, mean size and vertical distribution (percentage of individuals in the upper layer of the enclosures) of *Ceriodaphnia* and *Diaphanosoma* in the experimental enclosures. Values are medians calculated over three weeks, with the exception of vertical distribution, which was assessed only at the second week. The 25% and 75% quantiles are shown within brackets. NFS: fishless shallow enclosures; FS: fish in shallow enclosures; NFD: fishless deep enclosures; FD: fish in deep enclosures; FDR: fish in deep enclosures with a physical refuge for zooplankton. Modified from Bertolo et al. (1999a, b).</caption><thead><tr><th>Genus</th><th>NFS</th><th>FS</th><th>NFD</th><th>FD</th><th>FDR</th></tr></thead><tbody><tr><td>Abundance (ind L<sup>-1</sup>)</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><i>Ceriodaphnia</i></td><td>16.8 (12.8–40.8)</td><td>6.1 (4.5–6.2)</td><td>30.2 (26.3–43.5)</td><td>12.4 (9.1–12.5)</td><td>21.3 (20.8–27.8)</td></tr><tr><td><i>Diaphanosoma</i></td><td>10.7 (9.3–11.5)</td><td>7.4 (6.2–15.0)</td><td>2.9 (1.9–6.7)</td><td>6.7 (5.3–8.1)</td><td>2.5 (1.5–4.6)</td></tr><tr><td>Biomass (µg L<sup>-1</sup>)</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><i>Ceriodaphnia</i></td><td>19.8 (14.7–43.2)</td><td>3.9 (2.7–4.5)</td><td>36.2 (30.2–49.6)</td><td>8.7 (7.5–9.2)</td><td>19.5 (19.3–23.6)</td></tr><tr><td><i>Diaphanosoma</i></td><td>19.3 (18.7–23.2)</td><td>4.4 (3.7–8.9)</td><td>9.3 (5.8–14.5)</td><td>7.3 (5.5–7.7)</td><td>3.3 (2.1–4.8)</td></tr><tr><td>Body size (µm)</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><i>Ceriodaphnia</i></td><td>443.3 (440.4–455.9)</td><td>371.0 (355.9–375.8)</td><td>471.3 (469.3–472.0)</td><td>403.8 (397.6–411.7)</td><td>427.4 (417.8–434.7)</td></tr><tr><td><i>Diaphanosoma</i></td><td>638.6 (622.6–653.9)</td><td>480.7 (475.5–484.0)</td><td>726.0 (704.3–729.7)</td><td>591.7 (565.6–616.4)</td><td>617.3 (603.5–640.6)</td></tr><tr><td>Percentage in the upper layer</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><i>Ceriodaphnia</i></td><td>100</td><td>100</td><td>33.0 (27.8–39.9)</td><td>66.7 (63.3–70.2)</td><td>2.6 (2.0–19.7)</td></tr><tr><td><i>Diaphanosoma</i></td><td>100</td><td>100</td><td>58.1 (29.1–59.9)</td><td>20.0 (15.5–37.8)</td><td>41.7 (20.8–53.1)</td></tr></tbody></table>

because *Diaphanosoma* was relatively more abundant in the bottom layers of the experimental enclosure independently of the presence of fish or refugia.

### Background information: effects of depth on light limitation

We had previously shown that our deep enclosures were light-limited (Bertolo et al. 1999a). These results suggested that, by increasing light limitation, depth was associated to relatively low phytoplankton biomass, independently of the grazing pressure by zooplankton.

Therefore, we expect that epibiont burden for a given host size would be higher in shallow than in deep enclosures.

### Data analysis

The biology of crustacean molting and the hierarchical structure of the data in this study system pose some challenges for the analysis of epibiont burden. First, in the absence of molting, epibiont burden could be expected to increase linearly with host body size. However, epibiont burdens are reduced to zero at regular intervals by molting, which occurs at different sizes in different individuals (Fig. 1a). This pattern of molting therefore introduces considerable variation in the relationship between burden and host body size at the population level (Fig. 1b, c and

Appendix: Fig. A1). Furthermore, intra-group correlations arise from the nested sampling design because measurements made on individuals from a given enclosure are not independent; these dependencies must be considered in the analysis. Finally, the analysis must take into account that the measurements of burden are on an ordered categorical scale.

To characterize the relationships between epibiont burden and experimental treatments, we used a hierarchical version of an ordered multinomial logit model (Johnson and Albert, 1999). This model for ordered outcomes is a generalized linear model based on a cumulative link function, which typically is assumed to be the cumulative distribution function from a normal or a logistic probability density. The model was formulated in terms of a continuous unobserved, or latent, variable $\omega$ the values of which are associated with the five possible categorical outcomes as follows:

$$Pr(y_i \geq j) = F(\tau_j - \omega_i), \quad j = 0, \dots, J-1$$

$$Pr(y_i = J) = 1 - F(\tau_{j-1} - \omega_i)$$

$$\omega_i = x_i \beta + \psi_k$$

$$\psi_k \sim N(0, \sigma^2)$$
<figure><img src="image_2.png" /><figcaption>Fig. 1. Effects of host molting on epibiont burden. Theoretical relationship between host body length and epibiont burden (counts): (a) single zooplankton host and (b) multiple hosts with asynchronized molting. Asynchronized molting events associated with a sudden drop of epibiont burden introduces substantial variation in the relationship: (c) example of noisy data from our experiment with *Colacium* burden (five categories) vs. *Diaphanosoma* body size [log<sub>e</sub>(µm)].</figcaption></figure>

where *k* indexes the 12 enclosures, *i* indexes individual hosts, *j* indexes the *J* = 5 ordinal response categories, *N*(*µ*, *σ*²) is the normal distribution with mean *µ* and variance *σ*², and *F* is the cumulative distribution function of the logistic density. The *y*ᵢ variable denotes the observed outcomes (abundance category for individual *i*), whereas *ω*ᵢ is a latent continuous variable whose value is determined by a set of fixed effects and a normally distributed random effect (*ψ*ᵢ) for the enclosure. The *τ*ᵢ parameters represent cutoff or threshold points that separate the outcomes (categories of abundance) (Appendix: Fig. A2). The *x*ᵢ represents a design matrix for the *p* treatment variables: log<sub>e</sub>(cladoceran length) (continuous), time (week number, categorical), enclosure size (deep or shallow, categorical), fish (presence or absence, categorical), refuge (presence or absence, categorical), and experiment-specific interactions between these variables. Effects coding was used for all categorical variables. The components of **β** = (*β*₁, ..., *β*ₚ)' are the regression coefficients associated with the treatment variables.

Inference was conducted in a Bayesian framework, which requires the specification of a set of prior distributions. We used diffuse priors for all parameters:

$$ \beta \sim N_p(\mathbf{0}, 10^8 \mathbf{I}_p) $$

$$ \tau_0 \sim N(0, 10^2) \ I(\tau_0 < \tau_1) $$

$$ \tau_j \sim N(0, 10^2) \ I(\tau_{j-1} < \tau_j < \tau_{j+1}), \quad j = 1, \dots, 2 $$

$$ \tau_3 \sim N(0, 10^2) \ I(\tau_2 < \tau_3) $$

$$ \sigma \sim U(0, 5), $$

where $N_p(\mu, \Sigma)$, is the multivariate normal distribution with mean vector $\mu$ and covariance matrix $\Sigma$, $I_p$ is the $p$-dimensional identity matrix, and $U_{(a,b)}$ is the uniform distribution with lower limit *a* and upper limit *b*. The indicator function $I(\cdot)$ is notational shorthand to indicate that the cutoff points must follow the constraint: $\tau_0 < \tau_1 < \tau_2 < \tau_3$.

All models were implemented in the R environment using the rjags package to access the JAGS sampling engine (Plummer 2014). We ran two parallel MCMC chains of 100,000 samples each. The first 50,000 iterations of each chain were discarded (burn-in) and the following 50,000 iterations were thinned (1 in 50) to yield 2000 samples from the posterior distribution. The Brooks-Gelman-Rubin criterion implemented in package CODA was used to check for convergence of the chains. Software code and data are
<table><caption>Table 2. Coefficients (mean and upper and lower limits of the 95% credibility interval) of models for size-adjusted epibiont burden as a function of time and the treatments enclosure size (shallow or deep) and fish (present or absent), for *Ceriodaphnia* and *Diaphanosoma*. Bold text indicates factors with credibility intervals excluding zero.</caption><thead><tr><th>Model term</th><th>Mean</th><th>Upper CI</th><th>Lower CI</th></tr></thead><tbody><tr><td><em>Ceriodaphnia</em></td><td></td><td></td><td></td></tr><tr><td>log<sub>e</sub>(length)</td><td>0.397</td><td>-0.162</td><td>0.937</td></tr><tr><td>week<sub>2</sub></td><td>0.066</td><td>-0.125</td><td>0.255</td></tr><tr><td>week<sub>3</sub></td><td>1.136</td><td>0.945</td><td>1.331</td></tr><tr><td>enclosure size</td><td>-0.057</td><td>-0.443</td><td>0.315</td></tr><tr><td>fish</td><td>-0.456</td><td>-0.811</td><td>-0.101</td></tr><tr><td>enclosure size × fish</td><td>0.128</td><td>-0.249</td><td>0.498</td></tr><tr><td>fish × week<sub>2</sub></td><td>0.131</td><td>-0.053</td><td>0.327</td></tr><tr><td>fish × week<sub>3</sub></td><td>-0.351</td><td>-0.543</td><td>-0.168</td></tr><tr><td><em>Diaphanosoma</em></td><td></td><td></td><td></td></tr><tr><td>log<sub>e</sub>(length)</td><td>1.403</td><td>0.926</td><td>1.890</td></tr><tr><td>week<sub>2</sub></td><td>0.441</td><td>0.262</td><td>0.619</td></tr><tr><td>week<sub>3</sub></td><td>1.159</td><td>0.961</td><td>1.361</td></tr><tr><td>enclosure size</td><td>0.074</td><td>-0.388</td><td>0.543</td></tr><tr><td>fish</td><td>-0.756</td><td>-1.207</td><td>-0.330</td></tr><tr><td>enclosure size × fish</td><td>0.098</td><td>-0.294</td><td>0.520</td></tr><tr><td>enclosure size × week<sub>2</sub></td><td>-0.139</td><td>-0.32</td><td>0.035</td></tr><tr><td>enclosure size × week<sub>3</sub></td><td>-0.427</td><td>-0.616</td><td>-0.244</td></tr><tr><td>fish × week<sub>2</sub></td><td>0.064</td><td>-0.118</td><td>0.250</td></tr><tr><td>fish × week<sub>3</sub></td><td>-0.171</td><td>-0.364</td><td>0.020</td></tr></tbody></table>

provided in the Supplement.

## RESULTS

### Effects of host body size and fish on epibiont burden

We found a positive relationship between host body length and epibiont load for both host genera when analyzing the three-week series (Tables 2 and 3). Whereas for *Ceriodaphnia* this relationship seems to be weak (CI including the zero value), the evidence is much stronger for *Diaphanosoma*, whose coefficients for body length differ from zero (Tables 2 and 3). Host body length had a positive effect on epibiont burden for both host genera in the analysis of epibiont vertical distribution (Appendix: Table A1). After controlling for host body size, we found clear negative effects of fish on epibiont burden of both cladoceran genera, as shown by the coefficients for the “fish” factor in three out of four models built (Tables 2 and 3; Figs. 2 and 3). Total host biomass was not included in the models because this variable was strongly correlated with host body length.

<table><caption>Table 3. Coefficients (mean and upper and lower limits of the 95% credibility interval) of models for size-adjusted epibiont burden as a function of time and the treatments refuge (presence or absence) and fish (present or absent), for *Ceriodaphnia* and *Diaphanosoma* in deep enclosures. Bold text indicates factors with credibility intervals excluding zero.</caption><thead><tr><th>Model term</th><th>Mean</th><th>Upper CI</th><th>Lower CI</th></tr></thead><tbody><tr><td><em>Ceriodaphnia</em></td><td></td><td></td><td></td></tr><tr><td>log<sub>e</sub>(length)</td><td>0.469</td><td>-0.060</td><td>0.997</td></tr><tr><td>week<sub>2</sub></td><td>0.683</td><td>0.485</td><td>0.882</td></tr><tr><td>week<sub>3</sub></td><td>-0.193</td><td>-0.485</td><td>0.077</td></tr><tr><td>refuge</td><td>-0.220</td><td>-0.703</td><td>0.322</td></tr><tr><td>fish</td><td>-0.572</td><td>-1.216</td><td>-0.037</td></tr><tr><td>week<sub>2</sub> × refuge</td><td>0.985</td><td>0.710</td><td>1.268</td></tr><tr><td>week<sub>3</sub> × refuge</td><td>-0.690</td><td>-1.066</td><td>-0.305</td></tr><tr><td>week<sub>2</sub> × fish</td><td>0.465</td><td>0.191</td><td>0.756</td></tr><tr><td>week<sub>3</sub> × fish</td><td>-0.872</td><td>-1.333</td><td>-0.468</td></tr><tr><td><em>Diaphanosoma</em></td><td></td><td></td><td></td></tr><tr><td>log<sub>e</sub>(length)</td><td>0.791</td><td>0.224</td><td>1.370</td></tr><tr><td>week<sub>2</sub></td><td>0.756</td><td>0.553</td><td>0.966</td></tr><tr><td>week<sub>3</sub></td><td>-0.026</td><td>-0.257</td><td>0.222</td></tr><tr><td>refuge</td><td>-0.631</td><td>-1.320</td><td>0.089</td></tr><tr><td>Fish<sup>D</sup></td><td>-0.545</td><td>-1.391</td><td>0.220</td></tr><tr><td>week<sub>2</sub> × refuge</td><td>0.937</td><td>0.634</td><td>1.233</td></tr><tr><td>week<sub>3</sub> × refuge</td><td>-1.197</td><td>-1.589</td><td>-0.809</td></tr><tr><td>week<sub>2</sub> × fish</td><td>0.128</td><td>-0.136</td><td>0.401</td></tr><tr><td>week<sub>3</sub> × fish</td><td>-0.033</td><td>-0.383</td><td>0.318</td></tr></tbody></table>

### Effects of depth on light limitation

The analyses of the three-week time series on both deep and shallow enclosures with and without fish showed that epibiont load monotonically increased with time on both host genera (Fig. 2, Table 2). After controlling for the effect of body size, we observed a clear effect of fish in both shallow and deep enclosures for both host genera. Epibiont load was clearly higher in control enclosures (NFD and NFS), relatively to fish (FD and FS) (Table 2: coefficients involving the “fish” factor), and this negative effect of fish further increased on both host genera at the third week (Table 2: coefficients for “week<sub>3</sub> × fish” factor). *Ceriodaphnia* epibiont burden did not respond to the variations in enclosure depth (Table 2: coefficients including the “enclosure size” factor). In contrast, epibiont burden on *Diaphanosoma* was higher in shallow enclosures than in deep ones at the third week (Table 2: coefficient for the “enclosure size × week<sub>3</sub>” factor).

### Predation refuges and host vertical distribution

Whereas no clear differences among the treatments NFD, FD and FDR were observed
<figure><img src="image_3.png" /></figure>

Fig. 2. Fish predation vs. light limitation effects. Variation over time (weeks 1–3) of a proxy for individual epibiont burden (latent variable, $\omega = \beta X$, with the random effect $\psi$ set to its mean value, zero) in shallow (open symbols) and deep (dark symbols) enclosures in the presence (squares) or absence (circles) of fish. Data are adjusted for host body length. Horizontal dashed lines represent cutoffs or thresholds ($\tau$ values) associated with changes in epibiont burden categories (Appendix: Fig. A2). Upper panel: *Ceriodaphnia*; lower panel: *Diaphanosoma*.

during the first two weeks, a clear pattern emerged for both host genera at week three (Fig. 3). Compared to the control (NFD), the treatment with fish and a refuge for zooplankton

<figure><img src="image_4.png" /></figure>

Fig. 3. Zooplankton refuge use vs. epibiont burden. Variation over time (weeks 1–3) of a proxy for individual epibiont burden (latent variable, $\omega = \beta X$, with the random effect $\psi$ set to its mean value, zero) in deep enclosures. Results are shown for three treatments: absence of fish (circles); fish and refuge present (triangles); fish present, no refuge (squares). Data are adjusted for host body length. Horizontal dashed lines represent cutoffs or thresholds ($\tau$ values) associated with changes in epibiont burden categories (Appendix: Fig. A2). Upper panel: *Ceriodaphnia*; lower panel: *Diaphanosoma*.

(FDR) showed a clear reduction in epibiont burden for both *Ceriodaphnia* and *Diaphanosoma* (Fig. 3, Table 3). Epibiont burden in fish enclosures (FD) showed a similar pattern for
both genera, but resulted to be significant only for *Ceriodaphnia* (coefficients for “fish”, “week₂ × fish” and “week₃ × fish” in Table 3).

The analysis of the vertical distribution of zooplankton, which was conducted on data from week 2 only, allowed us to examine more closely the differences in vertical distribution of epibionts in the deep enclosures. This analysis revealed that *Diaphanosoma*, but not *Ceriodaphnia*, carried more epibionts in the surface layers (0–2 m depth) than in the bottom layers (2–4 m depth). In contrast, only *Ceriodaphnia* showed a positive effect of the presence of refuge on its epibiont burden (Appendix: Fig. A3 and Table A1). However, this effect was small when compared with the overall effect observed on *Ceriodaphnia* epibiont burden at the end of the experiment (Fig. 3), when the presence of the refuge was clearly associated to a reduction of *Colacium* burden compared to the control.

DISCUSSION

Our results clearly confirm the existence of a shared doom effect induced by fish predation on both zooplankton host genera and their epibionts. Our experiments also show that light penetration in the water column and host behavior have the potential to control the photosynthetic epibiont burden in semi-natural conditions.

Effects of host body size and fish
on epibiont burden

The existence of a clear negative effect of fish
after controlling for host body size highlights the
fact that fish not only selected larger host
individuals, but also those with heavier epibiont
burdens. Previous results on the effects of
zooplanktivorous fish on epibiont prevalence
suggested a similar mechanism (Willey et al.
1990), but could not demonstrate it directly
because host body size was not controlled for in
the analyses. We avoided this shortcoming since
in our models size-selectivity and the shared
doom effect were explicitly taken into account
and treated separately (i.e., “log~e~(length)” and
“fish” terms in Tables 2–3, and Appendix: Table
A1). Therefore, our results clearly suggest that
epibiosis can strengthen trophic interactions be-
tween fish and zooplankton, with potential effects

for both host and epibiont population dynamics.
Previous work has demonstrated that by selecting
heavily infected hosts, predators have the poten-
tial to shape prey demographics, and, in turn, to
control the spread of parasites (Pulkkinen and
Ebert 2006). In *Daphnia*, size-selective removal of
individuals has the potential to control the
persistence of parasites in the population (Bittner
et al. 2002).

Other examples of how epibionts can modu-
late trophic interactions can be found in the
literature (e.g., Wahl 2008a). As in our case,
epibiosis has been shown to increase predation
risk in a number of taxa, but the opposite effect is
also possible (Wahl 2008a), as shown by epibiotic
limpets that lower the vulnerability of their
mussel host to starfish predation (Thieltges
2005), and by epibiotic sponges that reduce the
vulnerability of the marine bivalve *Arco noae*
against predators (Marin and Belluga 2005). In
consequence, by either strengthening or weaken-
ing trophic interactions, epibiosis has the poten-
tial to generate community-wide effects, as
suggested by Wahl (2008a). In our model system,
epibionts have thus the potential to enhance the
top-down effects of planktivorous fish on zoo-
plankton, with potential structuring effects at the
community level as well as cascading effects on
lower trophic levels.

Effects of depth on light limitation

Our results also support our initial hypothesis
on light limitation of photosynthetic epibiont
burden in our experimental enclosures. We
observed a higher epibiont burden on *Diaphano-
soma* in shallow enclosures than in deep ones
(i.e., lower vs. higher light limitation conditions,
respectively), independently of fish predation
and host body size. However, this effect was
not observed in *Ceriodaphnia*. The observed
difference in response to light limitation between
the two host genera could probably be explained
in terms of host behavior. In fact, *Diaphanosoma*
used the part of the water column below 2 m
when possible (i.e., in deep enclosures only),
independently from the presence or absence of
fish. This created a contrast in host vertical
distribution between shallow and deep enclo-
sures and increased the likelihood of detecting
the effect of light limitation for this host genera.
*Ceriodaphnia*, in contrast, had a slightly greater
epibiont burden in shallow enclosures, but only
in the absence of fish. The complete lack of
response of *Ceriodaphnia* to light limitation in fish
enclosures might be explained by a shift towards
the shallower part of deep enclosures when fish
where present, thus reducing light limitation.

Predation refuges and host vertical distribution

In agreement with our initial hypothesis, the
refuge against fish predation did not allow
epibionts on *Ceriodaphnia* to maintain a burden
intermediate between those of fish and fishless
enclosures, despite the potential for a reduced
shared doom effect. Although the refuge was
effective in maintaining a relatively high abun-
dance of potential hosts for *Colacium* even in the
presence of fish, it did not seem to benefit the
epibionts. The epibiont burden on *Ceriodaphnia*
was in fact similar in the two fish treatments
(deep enclosures), independently of the presence
of refuge. Therefore, an overall weaker predation
pressure in the enclosures with refuge did not
appear to result in a smaller shared doom effect.
Although it is possible that the shared doom
effect was in fact similar with or without the
refuge because of a threshold effect, it seems
more likely that this similarity was related to the
shift in vertical distribution of *Ceriodaphnia* in the
presence of refuge. The vertical distribution of
*Ceriodaphnia* in the presence of fish was clearly
affected by the presence of the refuge: aggregat-
ing in the lower and safer part of the enclosures
probably increased light limitation for *Colacium*
on *Ceriodaphnia*.

Alternatively, these results might be partly due
to a weaker response to light limitation in
*Ceriodaphnia* than in *Diaphanosoma*, which would
hinder the detection of non-consumptive effects.
However, the observed difference between epi-
biont burden responses to light limitation in the
two host genera is interesting per se. After
controlling for body size, differences in key
biological traits of the host genera, such as
behavior, are likely to explain the differences in
epibiont burden among hosts and deserve more
attention in the future. A similar overall effect of
the refuge on *Colacium* burden was found for
*Diaphanosoma*, but in this case we did not expect
any non-consumptive effect due to host behav-
iour. The vertical position of *Diaphanosoma*, and
thus its average exposure to light, were in fact

similar in the two fish treatments in the deep
enclosures, and no major differences between
treatments in either predation pressure or light
limitation should be expected. Unfortunately, the
interpretation of results on the vertical distribu-
tion of *Colacium* burden (Appendix: Fig. A3 and
Table A1) has limited scope in the comparison
among treatments because, in contrast to week 3,
on week 2 there were no marked differences
among the treatments (see Figs. 2 and 3).
Nevertheless, these results give some extra
support to the light limitation hypothesis at the
within-treatment level since the *Colacium* burden
was higher in surface compared to bottom
samples, at least in *Diaphanosoma*.

Conclusions

Beside explicitly confirming the existence of a
shared doom effect and the role of environmental
factors in the control of epibiont populations, our
study showed that host behavior has the poten-
tial to control the epibiont burden in semi-natural
conditions. To our knowledge, this is the first
demonstration of epibiont control by host behav-
ior since a similar effect was suggested by
Threlkeld et al. (1993). These authors suggested
that host behaviours such as modulation of
vertical distribution might control the epibiont
burden via light limitation. Such non-consump-
tive effects are often underestimated, but might
have profound implications for community and
food-web dynamics (Kéfi et al. 2012). Under-
standing the potential consequences of this result
for the host in terms of control of the costs related
to the epibiont burden is a potentially rewarding
research avenue that merits further exploration.

Similar questions to those explored in our
work have been raised concerning *Daphnia*-
parasite interactions (Cáceres et al. 2014). For
example, Decaestecker et al. (2002) suggested
that *Daphnia* aggregation caused by vertical
migration can affect parasite transmission dy-
namics. By concentrating near pond sediments to
avoid fish predators, *Daphnia* might in fact
increase their encounter rate with parasite spores
(the “deep trouble hypothesis”; Decaestecker et
al. 2002). As a consequence of the presence of
multiple enemies (fish and parasites), habitat
selection behavior in *Daphnia* could be driven by
a tradeoff between predator and parasite avoid-
ance. However, host-epibiont interactions are
often complex and predicting their outcome is not always straightforward (Wahl 2008a). Our study system may not conform to the deep trouble hypothesis because in our experiments deeper layers are associated to both lower photosynthetic epibiont burden and predation risk. Taken together, these examples show how host-epibiont interactions can be complex and depend on the specific host-epibiont/parasite association examined. More generally, these and previous (Bertolo et al. 2010) experimental results confirm that fish predation has much more complex effects on primary producers that the classically observed increase in phytoplankton biomass (see Hulot et al. 2014) through a trophic cascade via zooplankton.

Epibionts are common on zooplankton, which are a unique and generally neglected habitat. Given the potential impact of interactions between epibionts and their zooplankton hosts on ecosystem processes such as respiration (Tang et al. 2010) and carbon recycling (Tang et al. 2010, Bickel et al. 2012), it is important to frame these interactions within a wider perspective. Future work should help to better understand the effects of predation and competition on the spatial distribution of hosts and their parasites and epibionts within lakes and to reveal potential feedback mechanisms.

## ACKNOWLEDGMENTS

We thank Alexandra M. Schmidt for discussion on an earlier draft of this work. A. Bertolo acknowledges support by the "Fonds d'Animation de la Recherche" of UQTR (FAR Project "Ecologie et évolution des réseaux d'interaction en milieux aquatiques peu profonds"). G. Lacroix was supported by the French National Research Agency (ANR BLANC, PHYT-BACK project 10-BLAN-1709-01). The preparation of the International Programs For Scientific Cooperation (project PICS06763), supported by the French National Center of Scientific Research, stimulated the publication of the paper. M. A. Rodríguez acknowledges the support of the Natural Sciences and Engineering Research Council of Canada. A. Bertolo and G. Lacroix conceived and conducted the experiments. M. A. Rodríguez conducted the statistical analysis. A. Bertolo, G. Lacroix and M. A. Rodríguez contributed in writing the paper.

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SUPPLEMENTAL MATERIAL

ECOLOGICAL ARCHIVES

The Appendix and the Supplement are available online: http://dx.doi.org/10.1890/ES14-00451.1.sm