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Bates et al 07
Journal of Experimental Marine Biology and Ecology 344 (2007) 206 – 214
www.elsevier.com/locate/jembe
Do changes in seaweed biodiversity influence
associated invertebrate epifauna?
Colin R. Bates ⁎, Robert E. DeWreede
Department of Botany, University of British Columbia, Department of Botany, 3529-6270 University Blvd. Vancouver, B.C., Canada V6T 1Z4
Bamfield Marine Sciences Centre, Bamfield, B.C., Canada V0R 1B0
Received 17 August 2006; received in revised form 8 January 2007; accepted 17 January 2007
Abstract
Most investigations of biogenic habitat provision consider the promotion of local biodiversity by single species, yet habitat-
forming species are often themselves components of diverse assemblages. Increased prevalence of anthropogenic changes to
assemblages of habitat-forming species prompts questions about the importance of facilitator biodiversity to associated organisms.
We used observational and short-term (30 days) manipulative studies of an intertidal seaweed system to test for the implications of
changes in four components of biodiversity (seaweed species richness, functional group richness, species composition, and
functional group composition) on associated small mobile invertebrate epifauna. We found that invertebrate epifauna richness and
abundance were not influenced by changes in seaweed biodiversity. Invertebrate assemblage structure was in most cases not
influenced by changes in seaweed biodiversity; only when algal assemblages were composed of monocultures of species with
‘foliose’ morphologies did we observe a difference in invertebrate assemblage structure. Correlations between algal functional
composition and invertebrate assemblage structure were observed, but there was no correlation between algal species composition
and invertebrate assemblage structure. These results suggest that changes in seaweed biodiversity are likely to have implications for
invertebrate epifauna only under specific scenarios of algal change.
© 2007 Elsevier B.V. All rights reserved.
Keywords: Composition; Facilitation; Functional groups; Morphology; Seaweeds; Species richness
1. Introduction edged, particularly in marine systems (Bertness et al.,
1999; Bruno and Bertness, 2000; Stachowicz, 2001;
Local biodiversity is often positively influenced by Bruno et al., 2003). Biogenic habitat provision is most
the presence of habitat forming or habitat modifying often investigated as the creation or modification of
organisms (Thompson et al., 1996; Stachowicz, 2001). habitat by one species for a group of other species
The importance of biogenic habitat provision and of (Castilla et al., 2004; Wonham et al., 2005). However,
positive interactions in general is increasingly acknowl- many situations exist where habitat-forming species are
components of assemblages of taxa that can collectively
act as habitat (Bruno and Bertness, 2000; Stachowicz,
⁎ Corresponding author. Bamfield Marine Sciences Centre, Bam-
2001; Bruno et al., 2003). Investigations into assem-
field, B.C., Canada V0R 1B0. Tel.: +1 250 728 3301x251; fax: +1 250
728 3452.
blage-level influence on biogenic habitat provision are
E-mail addresses: colinba@interchange.ubc.ca (C.R. Bates), much less frequent and, where available, have yielded
dewreede@interchange.ubc.ca (R.E. DeWreede). mixed results, showing positive, negative, and neutral
0022-0981/$ - see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2007.01.002
C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214 207
relationships between facilitator diversity and diversity referred to as ‘green-tides’. These observed changes
of associated organisms (Bruno and Bertness, 2000). involve different components of biodiversity, including
These mixed results concerning habitat provision by the number and identity of seaweed species and
multi-species communities may stem from problems of functional groups. Because seaweeds are vital biogenic
defining facilitator diversity, because various compo- habitat providers for small mobile invertebrates, an
nents of diversity (e.g., richness, composition) can affect understanding of the relationships between different
processes differentially (Diaz and Cabido, 2001; components of seaweed diversity and invertebrate
Naeem, 2002) and it can be difficult to separate the diversity is important for predicting the implications of
effects of different components of diversity (Naeem and marine floristic change.
Wright, 2003). Biodiversity, as it relates to ecosystem Here, we ask (1) Is seaweed species richness posi-
functioning, can be defined in a variety of different tively correlated with invertebrate species richness and
ways, incorporating the number of species (Magurran, abundance? (2) Is seaweed functional richness positive-
1988; Petchey, 2000), the functional roles of the species ly correlated with invertebrate species richness and
(Tilman et al., 1997; Diaz and Cabido, 2001; Petchey abundance? (3) Does species composition of host sea-
and Gaston, 2002), and the identity of the species or the weed assemblages correlate with invertebrate assem-
functional groups that compose the assemblage. blage structure? and (4) Does functional composition of
While much work in biodiversity research has host seaweed assemblages correlate with invertebrate
focused on species richness as the independent variable, assemblage structure?
there is debate about the relative importance of species
richness, functional richness and species or functional 2. Materials and methods
group identity (Tilman et al., 1997; Bruno et al., 2005).
Here, we describe our efforts to address these concepts We initiated this study with observational collections
in an intertidal study system, where we test how varia- to determine natural levels of seaweed diversity and
tion in four seaweed assemblage-level parameters (i.e. structure of associated mobile epifauna. We then per-
seaweed species richness, functional group richness, formed manipulative experiments over 2 years to deter-
species composition, and functional group composition) mine the implications of varied combinations of seaweed
influences associated small mobile epifauna. Under- species richness, functional richness, and species and
standing the relative influence of these different functional composition on structure of associated mobile
components of biodiversity on biogenic habitat provi- epifaunal assemblages. This study was done in June to
sion is becoming increasingly important as human August over 2 years (2003–2004) at Nudibranch Pt.
activities continue to alter composition of biological (48°48.871′N, 125°10.338′W), in southern Barkley
communities and reduce diversity (Coleman and Sound, British Columbia, Canada. Nudibranch Pt. is a
Williams, 2002). Habitat loss has been pinpointed as relatively pristine site with gently sloping, semi wave-
the major cause of declining biodiversity (Tilman et al., exposed rocky reefs. Site preparation took place in April
1994), and the implications are compounded if habitat and May 2003 and observational and manipulative
forming species are lost. quadrats measured 16 × 47 cm, oriented perpendicular to
Anthropogenic changes in seaweed diversity have the water line. This quadrat size was chosen as a man-
been observed in nearshore marine environments from ageable area to sample, and made efficient use of trans-
many regions throughout the world, most notably in plant materials. A list of seaweed species used in
Europe (Schramm and Nienhuis, 1996) and in eastern observational and manipulative studies is given in
Canada (Lotze and Milewski, 2004; Bates et al., 2005). Table 1. Current taxonomic authorities can be found by
Anthropogenic stressors that result in changes in sea- consulting AlgaeBase (www.algaebase.org).
weed assemblages include eutrophication, silt deposi-
tion, trampling, habitat alienation, and harvest of 2.1. Defining seaweed functional groups
predators or herbivores. These stressors act by compro-
mising the basic requirements of marine algae, which To assign seaweed species into functional groups
include substrate to attach to, light and nutrients for (Table 1), we used functional form groupings following
photosynthesis, and potential for successful dispersal Steneck and Dethier (1994). Owing to transplant meth-
and recruitment. As a result, stressed algal assemblages od limitation (described below), we employed only four
often shift from mosaics of longer-lived, perennial algae of a possible seven seaweed functional groups (Table 1):
to assemblages dominated by ephemeral, fast growing, foliose, corticated foliose, leathery, and corticated terete
nutrient scavenging annuals (Lotze et al., 1999), often (i.e. rounded in cross section). As asserted by Farina
208 C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214
Table 1 immediately placed into separate zippered collection
List of algal species included in this study, with functional group bags. Samples were then frozen for a minimum of 24 h
assignment and whether they were encountered in the observational
study (O), used in the manipulative study (M) or both (B)
to euthanize epifauna before processing.
Taxon Functional group Inclusion
2.3. Manipulative experiment
Ahnfeltiopsis leptophyllum Leathery O
Analipus japonicus Corticated terete B
To separate the influence of seaweed species richness,
Callithamnion pikeanum Filamentous O
Ceramium pacificum Filamentous O functional richness, and functional composition on
Ceramium sp. Filamentous O associated invertebrate epifauna, we created seaweed
Chondracanthus exasperatus Leathery M communities that varied each of these parameters while
Fucus gardneri Leathery B holding the other variables constant. We use the approach
Gastroclonium subarticulatum Corticated terete M
of ‘synthetic removal experiments’ as described by
Halosaccion glandiforme Foliose B
Mastocarpus jardinii Leathery M Schmid et al. (2002), where the experimental design
Mastocarpus papillatus Leathery B includes intact communities and then omits certain
Mazzaella affinis Corticated foliose B species or groups of species to determine the effects.
Mazzaella splendens Corticated foliose B Prior to each transplant experiment, plots were scraped
Microcladia borealis Corticated terete O
clear of existing biota. We then composed five sets of
Microcladia coulteri Corticated terete O
Neorhodomela larix Corticated terete M experimental communities (n = 4 per treatment), each with
Odonthalia flocossa Corticated terete B a set of four transplanted ‘control’ plots. The control plots
Osmundea spectabilis Leathery O were based on the communities described in the observa-
Porphyra sp. Foliose B tional study, and each was composed of eight seaweed
Prionitis lanceolata Corticated terete B
species randomly selected across four functional groups.
Sargassum muticum Corticated terete M
Ulva fenestrata Foliose B
Ulva intestinalis Foliose M 2.4. Experimental treatments
Ulva linza Foliose B
Ulva stenophylla Foliose B Three variables were considered when determining
composition of seaweed treatment plots: Seaweed spe-
cies richness (S ), seaweed functional richness, (F ), and
et al. (2003), the functional/morphological approach in seaweed functional composition (FC). A fourth param-
marine algae has had variable support for a gradient of eter, seaweed species composition, was incorporated by
functional performance across groups, but the endpoints randomly selecting species within functional groups
are well established with fast growing opportunistic according to the guidelines described below. To describe
‘simple’ forms (i.e. the foliose group) at one end, and the functional composition of seaweed plots, we
slower-growing, typically later successional species classified assemblages as simple (only ‘foliose’ forms
with ‘complex’ thalli (i.e. corticated terete) at the other present), complex (only ‘corticated terete’ forms pres-
end. Our discussion of seaweed functional composition ent), or mixed (all four functional groups present). The
concentrates on the differences between these endpoints. treatments described below are summarized in Table 2.
2.2. Observational study Treatment 1 (T1) S = 4, F = 4, FC = mixed. Four seaweed
species were included in each plot. One species was
The purpose of the observational study was two-fold: randomly selected from each seaweed functional
to determine natural levels of seaweed species richness, group, ensuring all functional groups were repre-
functional richness, and total seaweed biomass to aid in sented. This treatment tested for the consequences of
the creation of realistic ‘controls’ for transplanted reduced species richness without the loss of func-
seaweed communities; and to obtain baseline descrip- tional richness. This treatment is referred to as a
tions of the relationships between seaweed community ‘mixed polyculture’.
parameters and invertebrate diversity. Observational Treatment 2 (T2) S = 1, F = 1, FC = foliose. Monocultures
quadrats were sampled in May 2003 by harvesting a of species randomly selected from the ‘foliose’
patch located 50 cm to the right of ten randomly selected functional group. We refer to this treatment as the
manipulative quadrats (described below). Within each ‘simple monoculture’. This treatment is comparable to
observational quadrat, each seaweed species present, the ‘green tide’ phenomenon, where seaweed assem-
along with associated invertebrates, was collected and blages are composed of fast growing, opportunistic
C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214 209
Table 2 The anchors provided a means of attaching malleable wire
Description of algal assemblage parameters used to compose control grids to the intertidal. Seaweed thalli selected for
and experimental plots
transplant were collected from within the study site and
Treatment Species Functional Functional Year defaunated by dipping in fresh water and shaking,
identity richness (S ) richness (F ) composition
(FC)
followed by visual inspection and picking of remaining
epifauna (Kelaher, 2002). Holdfasts of algae were woven
C: Control 8 4 Mixed 2003 and
into three-twist PVC rope, and then attached to the wire
2004
T1: Mixed 4 4 Mixed 2003 grids with nylon zip ties. Mean biomass of all transplanted
Polyculture plots was approximately equal (dry biomass = 10.25 g ±
T2: Simple 1 1 Foliose 2003 0.94 g) and was equivalent to the seaweed biomass of the
Monoculture observational plots (12.84 g ± 2.00 g). Algal percent cover
T3: Simple 6 1 Foliose 2004
was greater than 95% in all plots.
Polyculture
T4: Complex 1 1 Corticated 2004 Plots were established over 3 days and left in the field
Monoculture terete for 30 days. Plots were then harvested by collecting the
T5: Complex 6 1 Corticated 2004 total biomass of each species from each plot into separate
Polyculture terete zippered collection bags. Samples were frozen for a
N = 4 for each treatment; each treatment had four associated control minimum of 24 h to euthanize epifauna before processing.
plots.
2.6. Sample processing
algae typically from the Chlorophyte order Ulvales
(Middelboe and Sand-Jensen, 2000). To remove the epifauna from the host alga, each
Treatment 3 (T3) S = 6, F = 1, FC = foliose. Polycultures frozen seaweed thallus was removed from its bag and
of six species selected from the ‘foliose’ morpho- soaked in a dish with 500 mL of seawater to thaw. Most
type. We refer to this treatment as the ‘simple epifauna sank to the bottom of the dish, but each sample
polyculture’. This treatment tests for the influence of was also rubbed and visually inspected to remove re-
a low functional richness but high species richness. maining epifauna. Thalli with dense branching or fold-
Treatment 4 (T4) S = 1, F = 1, FC = corticated terete. ing were processed with additional attention. This
Monocultures of species selected from the ‘corti- approach was highly effective, and visual inspection
cated terete’ functional group. This treatment is with a dissecting microscope revealed few, if any,
comparable to a late-successional seaweed assem- epifauna remaining on the thalli. Because sessile
blage, where a slower-growing, competitively invertebrate individuals were relatively scarce (typically
dominant, robust morphotype is found, such as bryozoans or barnacles) and difficult to quantify as
the Chondracanthus canaliculatus monocultures number of individuals (in the case of the colonial
described by Dean and Connell (1987). We refer to bryozoans), our analyses are limited to mobile epifauna.
this treatment as the ‘complex monoculture’. Samples were sieved through a 0.2 mm screen to retain
Treatment 5 (T5) S = 6, F = 1, FC = corticated terete. epifauna, and then preserved in a 1.5 mL Eppendorf
Polycultures of six species selected from the tube containing 95% ethanol. Invertebrates were then
‘corticated terete’ morphotype. We refer to this enumerated as morphospecies (Oliver and Beattie,
treatment as the ‘complex polyculture’. 1996) and then later keyed to the highest taxonomic
resolution possible. Host thalli were dried at 80 °C for
Treatments 1 and 2 were run in 2003 and treatments 3 24 h, and then weighed to the nearest 0.01 g to quantify
to 5 were run in 2004. In each year, all treatment plots host biomass.
had an associated control plot, resulting in 8 control
plots in 2003 and 12 control plots in 2004. 2.7. Statistical analysis
2.5. Seaweed transplants Tests for the influence of seaweed species and
functional richness were performed using ordinary
We employed the transplant approach of Shaughnessy least squares regression for the observational study,
and DeWreede (2001) to create composite communities. and one-way ANOVAs for the manipulative study, in
To prepare for transplants, plots were first cleared of the both cases using invertebrate taxon richness and
existing flora and fauna, five holes were drilled into the abundance as response variables. We found that groups
rocky substratum, and masonry anchors were embedded. of control plots were not different within year (P N 0.25)
210 C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214
Fig. 1. nMDS plots of Bray–Curtis Similarity based on: A) seaweed taxonomic composition, B) seaweed functional composition, and C) associated
mobile invertebrate epifauna, from 2003 and 2004. C: Control, T1: mixed polyculture, T2: simple monoculture, T3: simple polyculture, T4: complex
monoculture, T5: complex polyculture. (See Table 2 and text for detailed descriptions of treatments). Dashed line indicates that treatment group is
different than control group (ANOSIM p b 0.05; Table 4).
so controls were pooled across treatments within each Non-parametric multivariate approaches (Clarke,
year (Underwood, 1997). Treatments were compared to 1993) were used to test for the influence of seaweed
control plots from the same year in which the treatment taxonomic and functional composition on invertebrate
was done. To account for increased likelihood of Type 1 composition. Similarity in species composition of
statistical errors, we used Bonferroni corrected critical invertebrate samples and seaweed transplant plots was
alpha values in cases where multiple comparisons were calculated on fourth-root transformed (invertebrates)
performed (Zar, 1999). For parametric tests, data were and root-transformed (seaweed) abundances using Bray
tested for normality (Anderson–Darling test) and homo- and Curtis (1957) similarities and visualized using non-
geneity of variance using Cochran's C (Underwood, metric multidimensional scaling (nMDS). To calculate
1997). If data did not conform, appropriate transforma- seaweed functional composition, total per-plot biomass
tions were applied (Zar, 1999). Parametric tests were of each seaweed species was summed into the
carried out using JMP 4.0.4 (SAS Institute Inc.). appropriate functional group before applying root
C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214 211
Table 3 variables, however no low-diversity seaweed plots were
ANOSIM results for manipulative experiment: comparisons of specific encountered; average seaweed species richness was
treatments to control plots for algal taxonomic composition (A), algal
functional composition (B), and composition of associated mobile
6.1 (±0.49) and average seaweed functional richness was
invertebrate epifauna (C) 2.90 (± 0.23). There was no correlation between seaweed
Treatment A: algal species B: algal C: invertebrate
species richness versus invertebrate species richness
compared composition functional species (P = 0.64, r2 = 0.17) or invertebrate abundance (P = 0.65,
to control composition composition r2 = 0.02), or between seaweed functional richness
Clarke's P Clarke's P Clarke's P versus invertebrate richness (P = 0.73, r2 = 0.03) and
R value R value R value invertebrate abundance (P = 0.57, r2 = 0.04). Further, no
T1 − 0.012 0.476 −0.071 0.605 0.250 0.071 correlation was observed between invertebrate assem-
T2 0.865 0.005 0.317 0.043 0.520 0.001 blage structure and either seaweed assemblage structure
T3 0.954 0.001 0.271 0.009 0.282 0.042 (Spearman rank correlation (rs) = 0.111, P = 0.232) or
T4 0.896 0.001 0.733 0.002 0.213 0.149 seaweed functional structure (rs = 0.019, P = 0.469). An
T5 0.903 0.001 0.491 0.002 − 0.055 0.573
average of 301.7 (±63.5 SE) invertebrates were found per
plot, with 3017 epifauna individuals across 61 in-
transformation and calculating Bray–Curtis similarity. vertebrate taxa enumerated in total.
Two techniques were used to assess the implications of
the different treatments for invertebrate composition: 3.2. Manipulative experiment
a) for the manipulative experiment, direct comparisons
between treatments and controls were made using None of the five seaweed treatments resulted in dif-
Analysis of Similarities (ANOSIM; Clarke, 1993), and ferences in invertebrate richness or invertebrate abun-
b) for both the observational and manipulative compo- dance compared to control plots (ANOVA, P2003 N 0.025,
nents, assessments of overall congruence in multivariate P2004 N 0.017). Across all treatment plots, a total of 9593
similarity patterns between seaweed functional and invertebrate individuals were encountered across 66 taxa.
species composition versus invertebrate species com- Mean per-plot invertebrate taxon richness ranged from 15
position were made using Mantel tests (Zar, 1999); here to 25, and mean per-plot abundance ranged from 110 to
we calculate Spearman rank correlation (Zar, 1999) 338 individuals.
between similarity matrices. Invertebrate composition in most of the treatments
Where significant differences between treatment and varied independently of seaweed composition. Inverte-
controls were indicated by the ANOSIM tests, biota re- brate assemblages from mixed polycultures (T1) were
sponsible for differences between groups were identified not significantly different from the 2003 controls
using Similarity Percentages (SIMPER; Clarke, 1993). (ANOSIM P N 0.025), and simple polycultures (T3),
Multivariate analyses were carried out using PRIMER complex monocultures (T4), and complex polycultures
software (Version 5.2, Primer-E, www.primer-e.org). (T5) were not significantly different from the 2004
controls (ANOSIM P N 0.017; Fig. 1C and Table 3C). In
3. Results only one treatment (simple monocultures, T2) did com-
position of invertebrate assemblages depend on the
3.1. Observational study identity of the seaweed treatment (ANOSIM, R = 0.520,
P b 0.001; Fig. 1C and Table 3C). SIMPER analysis
For the observational collections, no significant cor- indicated that differences in the abundance of amphi-
relations were observed between any of the measured pods accounted for 42% of the observed assemblage
Table 4
Summary of differences in abundance of major invertebrate taxa found on control plots versus monocultures of foliose seaweed (Group T2)
Order Control average abundance Group T2 average abundance Average dissimilarity Dissimilarity/SD % contribution to
overall dissimilarity
Amphipoda 198.17 118.25 19.83 1.38 42.15
Harpacticoida 39.50 19.25 7.41 1.44 15.75
Gastropoda 41.17 23.50 4.68 1.19 9.95
Patellogastropoda 13.50 2.50 2.21 1.60 4.71
Acarida 14.00 8.25 2.19 2.22 4.65
Polychaeta 9.50 6.75 1.93 2.60 4.10
212 C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214
Table 5
Spearman rank correlation values for tests of congruence between two seaweed assemblage descriptors versus assemblage structure of associated
invertebrate epifauna
Observational collections Manipulative experiment
Epifauna similarity versus: rs P rs (T1–T2) P(T1–T2) rs(T3–T5) P(T3–T5)
Seaweed taxonomic similarity 0.111 0.232 0.111 0.239 0.103 0.139
Seaweed functional similarity 0.19 0.469 0.275 0.013 0.196 0.017
dissimilarity between T2 and the control plots (Table 4), seaweed host identity (Gee and Warwick, 1994;
followed by harpacticoid copepods (∼ 16%), snails Chemello and Milazzo, 2002). Our results are similar
(∼10%) and limpets, mites, and polychaetes which to Parker et al. (2001) who showed that within a subtidal
each accounted for less than 5% of the differences. Northeast Atlantic estuarine seagrass/drift seaweed
Overall similarity relationships between seaweed community, plant composition was a strong predictor
taxonomic composition and invertebrate taxonomic of invertebrate community structure, while plant
composition (Fig. 1, Table 5) were not correlated in richness showed only a weak positive correlation with
2003 (rs = 0.111, P = 0.239) or in 2004 (rs = 0.103, P = diversity of invertebrate epifauna. Our results contrast
0.139). However, overall patterns of seaweed functional with similar studies undertaken in terrestrial habitats.
composition were correlated with patterns of inverte- Haddad et al. (2001) reported that insect species
brate taxonomic composition in both 2003 (rs = 0.275, richness was positively correlated with plant species
P = 0.013) and 2004 (rs = 0.196, P = 0.017). and functional richness in grassland ecosystems, and
Perner et al. (2003) reported that after the cessation of
4. Discussion pollution, herbivore richness was positively influenced
by subsequent increases in plant species and functional
We found that many of the tested components of richness.
seaweed diversity had no observable influence on diver- Given that stronger relationships have been observed
sity of associated invertebrate epifauna. In all cases, between diversity of plants and invertebrates in
invertebrate richness and abundance varied indepen- terrestrial systems, it is logical to ask why marine
dently of the manipulated qualities of host algal assem- algal diversity and associated epifauna are not more
blages. Invertebrate assemblage structure was different tightly linked. Terrestrial insects are often specialized to
between control plots and algal assemblages composed their host (Janz et al., 2001), whereas marine inverte-
with simple monocultures, but under none of the other brates tend to be much more generalized in their host
test scenarios. Congruence was detected between algal usage (Arrontes, 1999), although examples of marine
functional structure and invertebrate assemblages, but host specialization do exist (Sotka, 2005). In the absence
not between algal taxonomic structure and invertebrate of widespread host-specialization, marine epifauna are
assemblages. likely more amenable than insects to switch to a new
When compared alone, species of algae vary in host if host composition or richness were to change.
quality of habitat provision for epifauna, with complex- Why did invertebrates associated with simple mono-
ly branching algal species typically having a greater cultures differ compared to the controls? The majority of
diversity of associated invertebrate epifauna as com- studies relating host architectural complexity to epifau-
pared to algae with simple morphologies (Gee and na diversity conclude that host plants that are better at
Warwick, 1994; Chemello and Milazzo, 2002). In our providing predator-free space will have the highest
study we examined invertebrates associated with associated invertebrate diversity (Duffy and Hay, 1991;
various types of seaweed communities. All seaweed Arrontes, 1999). The species included in the foliose
plots composed with greater than one species had functional group tend to be of low structural complexity,
associated invertebrate epifauna assemblages that were with many species lacking branches or specialized
not different than control plots that contained eight structures. This lack of complexity may provide fewer
seaweed species. When seaweed plots were composed spaces for epifauna to hide from predators, which could
with only one species, results of epifauna compari- explain the different composition of amphipods, har-
sons depended on the functional identity of the sea- pacticoid copepods, gastropods, limpets, mites, and
weed monoculture. This latter result is consistent with polychaete worms observed in simple monocultures
previous investigations that link invertebrate diversity to (Table 4) compared to controls. However, structural
C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214 213
complexity can be difficult to define in a straightforward Acknowledgements
manner, and other characteristics besides branching may
influence an algal host's ability to provide predator-free We acknowledge the support of numerous willing
space. Several of the foliose seaweed species (e.g. field and laboratory assistants: L. Hassall, J. Collens, S.
Porphyra spp., Ulva fenestrata) exhibit highly folded Donald, N. Jue, H. Nguyen, E.F. Ojeda, S. Parries, K.
morphologies, which can also provide effective shelter Rutlidge, R. Saraga, D. Taylor, S. Toews, and T. Yim. We
for invertebrate epifauna. Fig. 1C shows that several of also thank staff at the Bamfield Marine Sciences Centre
the simple monoculture plots had associated inverte- for the technical support, and to the Huu-ay-aht First
brate epifauna assemblages that group closely with Nation for access to their territory. Helpful comments
those from the control plots. This suggests that from B. Starzomski, I. McGaw, L. White, and two
functional groupings may not be the most reliable anonymous reviewers substantially improved this man-
method of predicting a seaweed species performance as uscript. This research was supported by NSERC research
a host for invertebrate epifauna. Evidence exists to funds (# 9872-04) to R. DeWreede, and NSERC PGS-B
suggest that host species identity is particularly impor- and BMSC fellowships to C. Bates. [RH]
tant when abiotic conditions are stressful. For example,
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www.elsevier.com/locate/jembe
Do changes in seaweed biodiversity influence
associated invertebrate epifauna?
Colin R. Bates ⁎, Robert E. DeWreede
Department of Botany, University of British Columbia, Department of Botany, 3529-6270 University Blvd. Vancouver, B.C., Canada V6T 1Z4
Bamfield Marine Sciences Centre, Bamfield, B.C., Canada V0R 1B0
Received 17 August 2006; received in revised form 8 January 2007; accepted 17 January 2007
Abstract
Most investigations of biogenic habitat provision consider the promotion of local biodiversity by single species, yet habitat-
forming species are often themselves components of diverse assemblages. Increased prevalence of anthropogenic changes to
assemblages of habitat-forming species prompts questions about the importance of facilitator biodiversity to associated organisms.
We used observational and short-term (30 days) manipulative studies of an intertidal seaweed system to test for the implications of
changes in four components of biodiversity (seaweed species richness, functional group richness, species composition, and
functional group composition) on associated small mobile invertebrate epifauna. We found that invertebrate epifauna richness and
abundance were not influenced by changes in seaweed biodiversity. Invertebrate assemblage structure was in most cases not
influenced by changes in seaweed biodiversity; only when algal assemblages were composed of monocultures of species with
‘foliose’ morphologies did we observe a difference in invertebrate assemblage structure. Correlations between algal functional
composition and invertebrate assemblage structure were observed, but there was no correlation between algal species composition
and invertebrate assemblage structure. These results suggest that changes in seaweed biodiversity are likely to have implications for
invertebrate epifauna only under specific scenarios of algal change.
© 2007 Elsevier B.V. All rights reserved.
Keywords: Composition; Facilitation; Functional groups; Morphology; Seaweeds; Species richness
1. Introduction edged, particularly in marine systems (Bertness et al.,
1999; Bruno and Bertness, 2000; Stachowicz, 2001;
Local biodiversity is often positively influenced by Bruno et al., 2003). Biogenic habitat provision is most
the presence of habitat forming or habitat modifying often investigated as the creation or modification of
organisms (Thompson et al., 1996; Stachowicz, 2001). habitat by one species for a group of other species
The importance of biogenic habitat provision and of (Castilla et al., 2004; Wonham et al., 2005). However,
positive interactions in general is increasingly acknowl- many situations exist where habitat-forming species are
components of assemblages of taxa that can collectively
act as habitat (Bruno and Bertness, 2000; Stachowicz,
⁎ Corresponding author. Bamfield Marine Sciences Centre, Bam-
2001; Bruno et al., 2003). Investigations into assem-
field, B.C., Canada V0R 1B0. Tel.: +1 250 728 3301x251; fax: +1 250
728 3452.
blage-level influence on biogenic habitat provision are
E-mail addresses: colinba@interchange.ubc.ca (C.R. Bates), much less frequent and, where available, have yielded
dewreede@interchange.ubc.ca (R.E. DeWreede). mixed results, showing positive, negative, and neutral
0022-0981/$ - see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2007.01.002
C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214 207
relationships between facilitator diversity and diversity referred to as ‘green-tides’. These observed changes
of associated organisms (Bruno and Bertness, 2000). involve different components of biodiversity, including
These mixed results concerning habitat provision by the number and identity of seaweed species and
multi-species communities may stem from problems of functional groups. Because seaweeds are vital biogenic
defining facilitator diversity, because various compo- habitat providers for small mobile invertebrates, an
nents of diversity (e.g., richness, composition) can affect understanding of the relationships between different
processes differentially (Diaz and Cabido, 2001; components of seaweed diversity and invertebrate
Naeem, 2002) and it can be difficult to separate the diversity is important for predicting the implications of
effects of different components of diversity (Naeem and marine floristic change.
Wright, 2003). Biodiversity, as it relates to ecosystem Here, we ask (1) Is seaweed species richness posi-
functioning, can be defined in a variety of different tively correlated with invertebrate species richness and
ways, incorporating the number of species (Magurran, abundance? (2) Is seaweed functional richness positive-
1988; Petchey, 2000), the functional roles of the species ly correlated with invertebrate species richness and
(Tilman et al., 1997; Diaz and Cabido, 2001; Petchey abundance? (3) Does species composition of host sea-
and Gaston, 2002), and the identity of the species or the weed assemblages correlate with invertebrate assem-
functional groups that compose the assemblage. blage structure? and (4) Does functional composition of
While much work in biodiversity research has host seaweed assemblages correlate with invertebrate
focused on species richness as the independent variable, assemblage structure?
there is debate about the relative importance of species
richness, functional richness and species or functional 2. Materials and methods
group identity (Tilman et al., 1997; Bruno et al., 2005).
Here, we describe our efforts to address these concepts We initiated this study with observational collections
in an intertidal study system, where we test how varia- to determine natural levels of seaweed diversity and
tion in four seaweed assemblage-level parameters (i.e. structure of associated mobile epifauna. We then per-
seaweed species richness, functional group richness, formed manipulative experiments over 2 years to deter-
species composition, and functional group composition) mine the implications of varied combinations of seaweed
influences associated small mobile epifauna. Under- species richness, functional richness, and species and
standing the relative influence of these different functional composition on structure of associated mobile
components of biodiversity on biogenic habitat provi- epifaunal assemblages. This study was done in June to
sion is becoming increasingly important as human August over 2 years (2003–2004) at Nudibranch Pt.
activities continue to alter composition of biological (48°48.871′N, 125°10.338′W), in southern Barkley
communities and reduce diversity (Coleman and Sound, British Columbia, Canada. Nudibranch Pt. is a
Williams, 2002). Habitat loss has been pinpointed as relatively pristine site with gently sloping, semi wave-
the major cause of declining biodiversity (Tilman et al., exposed rocky reefs. Site preparation took place in April
1994), and the implications are compounded if habitat and May 2003 and observational and manipulative
forming species are lost. quadrats measured 16 × 47 cm, oriented perpendicular to
Anthropogenic changes in seaweed diversity have the water line. This quadrat size was chosen as a man-
been observed in nearshore marine environments from ageable area to sample, and made efficient use of trans-
many regions throughout the world, most notably in plant materials. A list of seaweed species used in
Europe (Schramm and Nienhuis, 1996) and in eastern observational and manipulative studies is given in
Canada (Lotze and Milewski, 2004; Bates et al., 2005). Table 1. Current taxonomic authorities can be found by
Anthropogenic stressors that result in changes in sea- consulting AlgaeBase (www.algaebase.org).
weed assemblages include eutrophication, silt deposi-
tion, trampling, habitat alienation, and harvest of 2.1. Defining seaweed functional groups
predators or herbivores. These stressors act by compro-
mising the basic requirements of marine algae, which To assign seaweed species into functional groups
include substrate to attach to, light and nutrients for (Table 1), we used functional form groupings following
photosynthesis, and potential for successful dispersal Steneck and Dethier (1994). Owing to transplant meth-
and recruitment. As a result, stressed algal assemblages od limitation (described below), we employed only four
often shift from mosaics of longer-lived, perennial algae of a possible seven seaweed functional groups (Table 1):
to assemblages dominated by ephemeral, fast growing, foliose, corticated foliose, leathery, and corticated terete
nutrient scavenging annuals (Lotze et al., 1999), often (i.e. rounded in cross section). As asserted by Farina
208 C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214
Table 1 immediately placed into separate zippered collection
List of algal species included in this study, with functional group bags. Samples were then frozen for a minimum of 24 h
assignment and whether they were encountered in the observational
study (O), used in the manipulative study (M) or both (B)
to euthanize epifauna before processing.
Taxon Functional group Inclusion
2.3. Manipulative experiment
Ahnfeltiopsis leptophyllum Leathery O
Analipus japonicus Corticated terete B
To separate the influence of seaweed species richness,
Callithamnion pikeanum Filamentous O
Ceramium pacificum Filamentous O functional richness, and functional composition on
Ceramium sp. Filamentous O associated invertebrate epifauna, we created seaweed
Chondracanthus exasperatus Leathery M communities that varied each of these parameters while
Fucus gardneri Leathery B holding the other variables constant. We use the approach
Gastroclonium subarticulatum Corticated terete M
of ‘synthetic removal experiments’ as described by
Halosaccion glandiforme Foliose B
Mastocarpus jardinii Leathery M Schmid et al. (2002), where the experimental design
Mastocarpus papillatus Leathery B includes intact communities and then omits certain
Mazzaella affinis Corticated foliose B species or groups of species to determine the effects.
Mazzaella splendens Corticated foliose B Prior to each transplant experiment, plots were scraped
Microcladia borealis Corticated terete O
clear of existing biota. We then composed five sets of
Microcladia coulteri Corticated terete O
Neorhodomela larix Corticated terete M experimental communities (n = 4 per treatment), each with
Odonthalia flocossa Corticated terete B a set of four transplanted ‘control’ plots. The control plots
Osmundea spectabilis Leathery O were based on the communities described in the observa-
Porphyra sp. Foliose B tional study, and each was composed of eight seaweed
Prionitis lanceolata Corticated terete B
species randomly selected across four functional groups.
Sargassum muticum Corticated terete M
Ulva fenestrata Foliose B
Ulva intestinalis Foliose M 2.4. Experimental treatments
Ulva linza Foliose B
Ulva stenophylla Foliose B Three variables were considered when determining
composition of seaweed treatment plots: Seaweed spe-
cies richness (S ), seaweed functional richness, (F ), and
et al. (2003), the functional/morphological approach in seaweed functional composition (FC). A fourth param-
marine algae has had variable support for a gradient of eter, seaweed species composition, was incorporated by
functional performance across groups, but the endpoints randomly selecting species within functional groups
are well established with fast growing opportunistic according to the guidelines described below. To describe
‘simple’ forms (i.e. the foliose group) at one end, and the functional composition of seaweed plots, we
slower-growing, typically later successional species classified assemblages as simple (only ‘foliose’ forms
with ‘complex’ thalli (i.e. corticated terete) at the other present), complex (only ‘corticated terete’ forms pres-
end. Our discussion of seaweed functional composition ent), or mixed (all four functional groups present). The
concentrates on the differences between these endpoints. treatments described below are summarized in Table 2.
2.2. Observational study Treatment 1 (T1) S = 4, F = 4, FC = mixed. Four seaweed
species were included in each plot. One species was
The purpose of the observational study was two-fold: randomly selected from each seaweed functional
to determine natural levels of seaweed species richness, group, ensuring all functional groups were repre-
functional richness, and total seaweed biomass to aid in sented. This treatment tested for the consequences of
the creation of realistic ‘controls’ for transplanted reduced species richness without the loss of func-
seaweed communities; and to obtain baseline descrip- tional richness. This treatment is referred to as a
tions of the relationships between seaweed community ‘mixed polyculture’.
parameters and invertebrate diversity. Observational Treatment 2 (T2) S = 1, F = 1, FC = foliose. Monocultures
quadrats were sampled in May 2003 by harvesting a of species randomly selected from the ‘foliose’
patch located 50 cm to the right of ten randomly selected functional group. We refer to this treatment as the
manipulative quadrats (described below). Within each ‘simple monoculture’. This treatment is comparable to
observational quadrat, each seaweed species present, the ‘green tide’ phenomenon, where seaweed assem-
along with associated invertebrates, was collected and blages are composed of fast growing, opportunistic
C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214 209
Table 2 The anchors provided a means of attaching malleable wire
Description of algal assemblage parameters used to compose control grids to the intertidal. Seaweed thalli selected for
and experimental plots
transplant were collected from within the study site and
Treatment Species Functional Functional Year defaunated by dipping in fresh water and shaking,
identity richness (S ) richness (F ) composition
(FC)
followed by visual inspection and picking of remaining
epifauna (Kelaher, 2002). Holdfasts of algae were woven
C: Control 8 4 Mixed 2003 and
into three-twist PVC rope, and then attached to the wire
2004
T1: Mixed 4 4 Mixed 2003 grids with nylon zip ties. Mean biomass of all transplanted
Polyculture plots was approximately equal (dry biomass = 10.25 g ±
T2: Simple 1 1 Foliose 2003 0.94 g) and was equivalent to the seaweed biomass of the
Monoculture observational plots (12.84 g ± 2.00 g). Algal percent cover
T3: Simple 6 1 Foliose 2004
was greater than 95% in all plots.
Polyculture
T4: Complex 1 1 Corticated 2004 Plots were established over 3 days and left in the field
Monoculture terete for 30 days. Plots were then harvested by collecting the
T5: Complex 6 1 Corticated 2004 total biomass of each species from each plot into separate
Polyculture terete zippered collection bags. Samples were frozen for a
N = 4 for each treatment; each treatment had four associated control minimum of 24 h to euthanize epifauna before processing.
plots.
2.6. Sample processing
algae typically from the Chlorophyte order Ulvales
(Middelboe and Sand-Jensen, 2000). To remove the epifauna from the host alga, each
Treatment 3 (T3) S = 6, F = 1, FC = foliose. Polycultures frozen seaweed thallus was removed from its bag and
of six species selected from the ‘foliose’ morpho- soaked in a dish with 500 mL of seawater to thaw. Most
type. We refer to this treatment as the ‘simple epifauna sank to the bottom of the dish, but each sample
polyculture’. This treatment tests for the influence of was also rubbed and visually inspected to remove re-
a low functional richness but high species richness. maining epifauna. Thalli with dense branching or fold-
Treatment 4 (T4) S = 1, F = 1, FC = corticated terete. ing were processed with additional attention. This
Monocultures of species selected from the ‘corti- approach was highly effective, and visual inspection
cated terete’ functional group. This treatment is with a dissecting microscope revealed few, if any,
comparable to a late-successional seaweed assem- epifauna remaining on the thalli. Because sessile
blage, where a slower-growing, competitively invertebrate individuals were relatively scarce (typically
dominant, robust morphotype is found, such as bryozoans or barnacles) and difficult to quantify as
the Chondracanthus canaliculatus monocultures number of individuals (in the case of the colonial
described by Dean and Connell (1987). We refer to bryozoans), our analyses are limited to mobile epifauna.
this treatment as the ‘complex monoculture’. Samples were sieved through a 0.2 mm screen to retain
Treatment 5 (T5) S = 6, F = 1, FC = corticated terete. epifauna, and then preserved in a 1.5 mL Eppendorf
Polycultures of six species selected from the tube containing 95% ethanol. Invertebrates were then
‘corticated terete’ morphotype. We refer to this enumerated as morphospecies (Oliver and Beattie,
treatment as the ‘complex polyculture’. 1996) and then later keyed to the highest taxonomic
resolution possible. Host thalli were dried at 80 °C for
Treatments 1 and 2 were run in 2003 and treatments 3 24 h, and then weighed to the nearest 0.01 g to quantify
to 5 were run in 2004. In each year, all treatment plots host biomass.
had an associated control plot, resulting in 8 control
plots in 2003 and 12 control plots in 2004. 2.7. Statistical analysis
2.5. Seaweed transplants Tests for the influence of seaweed species and
functional richness were performed using ordinary
We employed the transplant approach of Shaughnessy least squares regression for the observational study,
and DeWreede (2001) to create composite communities. and one-way ANOVAs for the manipulative study, in
To prepare for transplants, plots were first cleared of the both cases using invertebrate taxon richness and
existing flora and fauna, five holes were drilled into the abundance as response variables. We found that groups
rocky substratum, and masonry anchors were embedded. of control plots were not different within year (P N 0.25)
210 C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214
Fig. 1. nMDS plots of Bray–Curtis Similarity based on: A) seaweed taxonomic composition, B) seaweed functional composition, and C) associated
mobile invertebrate epifauna, from 2003 and 2004. C: Control, T1: mixed polyculture, T2: simple monoculture, T3: simple polyculture, T4: complex
monoculture, T5: complex polyculture. (See Table 2 and text for detailed descriptions of treatments). Dashed line indicates that treatment group is
different than control group (ANOSIM p b 0.05; Table 4).
so controls were pooled across treatments within each Non-parametric multivariate approaches (Clarke,
year (Underwood, 1997). Treatments were compared to 1993) were used to test for the influence of seaweed
control plots from the same year in which the treatment taxonomic and functional composition on invertebrate
was done. To account for increased likelihood of Type 1 composition. Similarity in species composition of
statistical errors, we used Bonferroni corrected critical invertebrate samples and seaweed transplant plots was
alpha values in cases where multiple comparisons were calculated on fourth-root transformed (invertebrates)
performed (Zar, 1999). For parametric tests, data were and root-transformed (seaweed) abundances using Bray
tested for normality (Anderson–Darling test) and homo- and Curtis (1957) similarities and visualized using non-
geneity of variance using Cochran's C (Underwood, metric multidimensional scaling (nMDS). To calculate
1997). If data did not conform, appropriate transforma- seaweed functional composition, total per-plot biomass
tions were applied (Zar, 1999). Parametric tests were of each seaweed species was summed into the
carried out using JMP 4.0.4 (SAS Institute Inc.). appropriate functional group before applying root
C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214 211
Table 3 variables, however no low-diversity seaweed plots were
ANOSIM results for manipulative experiment: comparisons of specific encountered; average seaweed species richness was
treatments to control plots for algal taxonomic composition (A), algal
functional composition (B), and composition of associated mobile
6.1 (±0.49) and average seaweed functional richness was
invertebrate epifauna (C) 2.90 (± 0.23). There was no correlation between seaweed
Treatment A: algal species B: algal C: invertebrate
species richness versus invertebrate species richness
compared composition functional species (P = 0.64, r2 = 0.17) or invertebrate abundance (P = 0.65,
to control composition composition r2 = 0.02), or between seaweed functional richness
Clarke's P Clarke's P Clarke's P versus invertebrate richness (P = 0.73, r2 = 0.03) and
R value R value R value invertebrate abundance (P = 0.57, r2 = 0.04). Further, no
T1 − 0.012 0.476 −0.071 0.605 0.250 0.071 correlation was observed between invertebrate assem-
T2 0.865 0.005 0.317 0.043 0.520 0.001 blage structure and either seaweed assemblage structure
T3 0.954 0.001 0.271 0.009 0.282 0.042 (Spearman rank correlation (rs) = 0.111, P = 0.232) or
T4 0.896 0.001 0.733 0.002 0.213 0.149 seaweed functional structure (rs = 0.019, P = 0.469). An
T5 0.903 0.001 0.491 0.002 − 0.055 0.573
average of 301.7 (±63.5 SE) invertebrates were found per
plot, with 3017 epifauna individuals across 61 in-
transformation and calculating Bray–Curtis similarity. vertebrate taxa enumerated in total.
Two techniques were used to assess the implications of
the different treatments for invertebrate composition: 3.2. Manipulative experiment
a) for the manipulative experiment, direct comparisons
between treatments and controls were made using None of the five seaweed treatments resulted in dif-
Analysis of Similarities (ANOSIM; Clarke, 1993), and ferences in invertebrate richness or invertebrate abun-
b) for both the observational and manipulative compo- dance compared to control plots (ANOVA, P2003 N 0.025,
nents, assessments of overall congruence in multivariate P2004 N 0.017). Across all treatment plots, a total of 9593
similarity patterns between seaweed functional and invertebrate individuals were encountered across 66 taxa.
species composition versus invertebrate species com- Mean per-plot invertebrate taxon richness ranged from 15
position were made using Mantel tests (Zar, 1999); here to 25, and mean per-plot abundance ranged from 110 to
we calculate Spearman rank correlation (Zar, 1999) 338 individuals.
between similarity matrices. Invertebrate composition in most of the treatments
Where significant differences between treatment and varied independently of seaweed composition. Inverte-
controls were indicated by the ANOSIM tests, biota re- brate assemblages from mixed polycultures (T1) were
sponsible for differences between groups were identified not significantly different from the 2003 controls
using Similarity Percentages (SIMPER; Clarke, 1993). (ANOSIM P N 0.025), and simple polycultures (T3),
Multivariate analyses were carried out using PRIMER complex monocultures (T4), and complex polycultures
software (Version 5.2, Primer-E, www.primer-e.org). (T5) were not significantly different from the 2004
controls (ANOSIM P N 0.017; Fig. 1C and Table 3C). In
3. Results only one treatment (simple monocultures, T2) did com-
position of invertebrate assemblages depend on the
3.1. Observational study identity of the seaweed treatment (ANOSIM, R = 0.520,
P b 0.001; Fig. 1C and Table 3C). SIMPER analysis
For the observational collections, no significant cor- indicated that differences in the abundance of amphi-
relations were observed between any of the measured pods accounted for 42% of the observed assemblage
Table 4
Summary of differences in abundance of major invertebrate taxa found on control plots versus monocultures of foliose seaweed (Group T2)
Order Control average abundance Group T2 average abundance Average dissimilarity Dissimilarity/SD % contribution to
overall dissimilarity
Amphipoda 198.17 118.25 19.83 1.38 42.15
Harpacticoida 39.50 19.25 7.41 1.44 15.75
Gastropoda 41.17 23.50 4.68 1.19 9.95
Patellogastropoda 13.50 2.50 2.21 1.60 4.71
Acarida 14.00 8.25 2.19 2.22 4.65
Polychaeta 9.50 6.75 1.93 2.60 4.10
212 C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214
Table 5
Spearman rank correlation values for tests of congruence between two seaweed assemblage descriptors versus assemblage structure of associated
invertebrate epifauna
Observational collections Manipulative experiment
Epifauna similarity versus: rs P rs (T1–T2) P(T1–T2) rs(T3–T5) P(T3–T5)
Seaweed taxonomic similarity 0.111 0.232 0.111 0.239 0.103 0.139
Seaweed functional similarity 0.19 0.469 0.275 0.013 0.196 0.017
dissimilarity between T2 and the control plots (Table 4), seaweed host identity (Gee and Warwick, 1994;
followed by harpacticoid copepods (∼ 16%), snails Chemello and Milazzo, 2002). Our results are similar
(∼10%) and limpets, mites, and polychaetes which to Parker et al. (2001) who showed that within a subtidal
each accounted for less than 5% of the differences. Northeast Atlantic estuarine seagrass/drift seaweed
Overall similarity relationships between seaweed community, plant composition was a strong predictor
taxonomic composition and invertebrate taxonomic of invertebrate community structure, while plant
composition (Fig. 1, Table 5) were not correlated in richness showed only a weak positive correlation with
2003 (rs = 0.111, P = 0.239) or in 2004 (rs = 0.103, P = diversity of invertebrate epifauna. Our results contrast
0.139). However, overall patterns of seaweed functional with similar studies undertaken in terrestrial habitats.
composition were correlated with patterns of inverte- Haddad et al. (2001) reported that insect species
brate taxonomic composition in both 2003 (rs = 0.275, richness was positively correlated with plant species
P = 0.013) and 2004 (rs = 0.196, P = 0.017). and functional richness in grassland ecosystems, and
Perner et al. (2003) reported that after the cessation of
4. Discussion pollution, herbivore richness was positively influenced
by subsequent increases in plant species and functional
We found that many of the tested components of richness.
seaweed diversity had no observable influence on diver- Given that stronger relationships have been observed
sity of associated invertebrate epifauna. In all cases, between diversity of plants and invertebrates in
invertebrate richness and abundance varied indepen- terrestrial systems, it is logical to ask why marine
dently of the manipulated qualities of host algal assem- algal diversity and associated epifauna are not more
blages. Invertebrate assemblage structure was different tightly linked. Terrestrial insects are often specialized to
between control plots and algal assemblages composed their host (Janz et al., 2001), whereas marine inverte-
with simple monocultures, but under none of the other brates tend to be much more generalized in their host
test scenarios. Congruence was detected between algal usage (Arrontes, 1999), although examples of marine
functional structure and invertebrate assemblages, but host specialization do exist (Sotka, 2005). In the absence
not between algal taxonomic structure and invertebrate of widespread host-specialization, marine epifauna are
assemblages. likely more amenable than insects to switch to a new
When compared alone, species of algae vary in host if host composition or richness were to change.
quality of habitat provision for epifauna, with complex- Why did invertebrates associated with simple mono-
ly branching algal species typically having a greater cultures differ compared to the controls? The majority of
diversity of associated invertebrate epifauna as com- studies relating host architectural complexity to epifau-
pared to algae with simple morphologies (Gee and na diversity conclude that host plants that are better at
Warwick, 1994; Chemello and Milazzo, 2002). In our providing predator-free space will have the highest
study we examined invertebrates associated with associated invertebrate diversity (Duffy and Hay, 1991;
various types of seaweed communities. All seaweed Arrontes, 1999). The species included in the foliose
plots composed with greater than one species had functional group tend to be of low structural complexity,
associated invertebrate epifauna assemblages that were with many species lacking branches or specialized
not different than control plots that contained eight structures. This lack of complexity may provide fewer
seaweed species. When seaweed plots were composed spaces for epifauna to hide from predators, which could
with only one species, results of epifauna compari- explain the different composition of amphipods, har-
sons depended on the functional identity of the sea- pacticoid copepods, gastropods, limpets, mites, and
weed monoculture. This latter result is consistent with polychaete worms observed in simple monocultures
previous investigations that link invertebrate diversity to (Table 4) compared to controls. However, structural
C.R. Bates, R.E. DeWreede / Journal of Experimental Marine Biology and Ecology 344 (2007) 206–214 213
complexity can be difficult to define in a straightforward Acknowledgements
manner, and other characteristics besides branching may
influence an algal host's ability to provide predator-free We acknowledge the support of numerous willing
space. Several of the foliose seaweed species (e.g. field and laboratory assistants: L. Hassall, J. Collens, S.
Porphyra spp., Ulva fenestrata) exhibit highly folded Donald, N. Jue, H. Nguyen, E.F. Ojeda, S. Parries, K.
morphologies, which can also provide effective shelter Rutlidge, R. Saraga, D. Taylor, S. Toews, and T. Yim. We
for invertebrate epifauna. Fig. 1C shows that several of also thank staff at the Bamfield Marine Sciences Centre
the simple monoculture plots had associated inverte- for the technical support, and to the Huu-ay-aht First
brate epifauna assemblages that group closely with Nation for access to their territory. Helpful comments
those from the control plots. This suggests that from B. Starzomski, I. McGaw, L. White, and two
functional groupings may not be the most reliable anonymous reviewers substantially improved this man-
method of predicting a seaweed species performance as uscript. This research was supported by NSERC research
a host for invertebrate epifauna. Evidence exists to funds (# 9872-04) to R. DeWreede, and NSERC PGS-B
suggest that host species identity is particularly impor- and BMSC fellowships to C. Bates. [RH]
tant when abiotic conditions are stressful. For example,
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