Saccate thallus of the red alga Halosaccion glandiforme harbor diverse invertebrate fauna
Saccate thallus of the red alga Halosaccion glandiforme harbor diverse invertebrate fauna
Ritindra N. Bhaduri . Maya Wolf 0
0 M. Wolf Oregon Institute of Marine Biology, University of Oregon , Charleston, OR 97420 , USA
Rocky intertidal zones are biologically diverse environments with numerous physical stressors; as such, close associations between organisms often develop to overcome such stressors and enhance survival of associates. As major components of rocky shores, macroalgae support numerous invertebrate species. In this study, we evaluated the habitat-providing role of the red alga, Halosaccion glandiforme (S.G. Gmelin) Ruprecht. This alga, also called sea sacs, is commonly found on rocky shores along the West Coast of North America. During emersion, this seaweed holds water within its saccate thallus, which can potentially serve as microhabitat for various organisms. Little is known about the composition of microfauna associated with this seaweed; as such, we documented richness and abundance of species found inside its thallus. Algal specimens were collected from Charleston, Oregon and transported to the laboratory for further analyses. Of the 119 thalli examined, 12 taxa were documented. Nematodes and copepods were the dominant taxa. Other groups represented included ostracods, turbellarians, halacarid mites, bivalves, rotifers, and three larval types (barnacle cyprids, copepod nauplii, mollusc veliger). Diatoms, crustacean molt remnants, detritus, and sand particles were also observed inside thalli. Species richness and abundance were positively correlated with thalli volume, as well as intra-thalli fluid volume. Several feeding and other behaviors of colonizers were noted; they included herbivory, predator-prey interactions, detritivory, and molting. Our findings demonstrate that H. glandiforme provide refuge for organisms from harsh environmental conditions during emersion periods, and also serve as feeding and nursery grounds for its diverse invertebrate fauna.
Sea sacs; Microhabitat; Invertebrate composition; Rocky intertidal community
Rocky shores are dynamic environments inhabited by organisms that are able to withstand harsh abiotic and
biotic conditions. Some of these organisms, especially macroalgae, provide habitats for many benthic species.
These species depend on the physical structure and other resources provided by the seaweeds, thereby enhancing
their survival and increasing diversity and abundance (Lilley and Schiel 2006; Wikstro¨m and Kautsky 2007).
Size and morphological features of seaweeds can have a major bearing on the benefits they provide to other
species. Numerous invertebrates are dependent on seaweeds with varying morphological features, including
the complex three-dimensional Macrocystis (Graham 2004), the compact spongy Codium (Trowbridge 1998;
Bulleri et al. 2006), the fan-like broad thallus of Chondrus (Janiak and Whitlatch 2012), the crustose coralline
algae Clathromorphum (Chenelot et al. 2011) and the calcareous rhodoliths (Foster 2001). Steller et al. (2003)
reported that the total number of organisms supported by the coralline red algal rhodoliths significantly
increased with both complexity (branching density) and space available (thallus volume) when compared with
adjacent sand community. Thus, thallus size/volume can be a factor determining species richness and
abundance in associated organisms.
Another morphological trait found in some algae is the presence of saccate or sac-like thallus that retains
sea water when exposed to air during low tide. The saccate red alga Halosaccion glandiforme grows in clumps
in the rocky intertidal areas along the Pacific coast of North America, ranging from the northern Aleutian Isles
to southern California (Mondragon 2003). The plant has a short stipe, a discoid holdfast, and thalli measuring
3–4 cm in diameter; it grows to a length of 10–20 cm over the course of a year (Johnson 1994). This seaweed
is commonly referred to as the sea sac because its thallus is a cylindrical hollow sac, partially filled with sea
water and about a cubic centimeter of gas. Each thallus possesses 5–15 irregularly shaped pores, 10–200 lm
in diameter, which allow water into and out of the thallus during exposure and immersion associated with tidal
cycles (DePamphilis 1978; Vogel and Loudon 1985). When tides recede, water inside the thallus is retained.
Such water reserves reduce desiccation and heating of tissue during periods of emersion (DePamphilis 1978).
It has been reported in some field guides that the water-filled sacs of H. glandiforme are inhabited by a variety
of invertebrates (Mondragon 2003; Lamb and Hanby 2005).
The role of this ‘‘sea sac’’ as a microhabitat for assemblages of small invertebrates has been virtually
unexplored. In this study, for the first time, we note the presence of fauna found inside the saccate thallus of H.
glandiforme. The objectives of this study were to: (1) quantify species richness and abundance (2) determine
relationship between species richness/abundance and thallus/seawater volume using multiple regression, and
(3) observe miscellaneous ecological interactions between taxa.
Fronds of H. glandiforme were collected from Cape Arago State Park in Charleston, Oregon (43.3062 N;
124.3935 W), USA, between July and September 2015, during low tide. During sampling, the short stipe was
gently snipped using a scalpel while making sure the water-filled thalli were intact (Fig. 1). The seaweeds
Fig. 1 Saccate thallus of Halosaccion glandiforme, tapering to a short stipe and attached to rocks with small discoidal holdfast.
Note the oblong sac partially filled with seawater
were transferred to plastic containers and transported to the laboratory at the Oregon Institute of Marine
Biology for further analysis. Any damaged or dehydrated thalli were discarded and not analyzed in our study.
All analyses were performed within 8 h of collection, which ensured quantifying and observing live fauna.
Using dissecting scissors, each thallus was carefully removed from the stipe. Assuming that each
waterfilled thallus was roughly columnar in shape, we measured thallus volume using the formula V = pr2h, where
h was the length and r was the width at the widest point on the thallus. The thin seawater-filled sac was held
vertically and the tip of the thallus was cut with a scissor. To measure seawater volume, the internal water was
withdrawn using a calibrated 5 cc wide mouth syringe. The content of the syringe was transferred into a watch
glass and examined for fauna under a binocular stereo microscope (Olympus 10X). Most specimens were
identified as close to their taxonomic level as possible using available taxonomic keys (Light and Carlton
2007) and their abundance noted. 10 min were spent observing interactions (if any) between the colonizers for
each thallus. Other recognizable intra-thallus components (e.g., phytoplankton, detritus, molt remnants, etc.)
were also noted for documenting additional ecological associations.
Multiple regression analyses were performed to determine the relationship between the richness and
abundance of the invertebrate fauna and the size of the sea sacs, which included thallus size and fluid volume
within each sac. A Kolmogorov–Smirnov test showed the data were not normally distributed, and further
transformation did not normalize the data. However, linear regression/correlation might still be robust to
nonnormality (McDonald 2014), so analyses were performed despite this violation. P values \ 0.05 were
considered statistically significant.
We examined a total of 119 thalli of H. glandiforme. Table 1 lists the different types of invertebrates and their
numbers associated with this alga. Of the 119 thalli inspected, 99 (83%) were colonized by 845 individuals
Table 1 Richness, abundance (A), % occurrence (O), mean occurrence (M.O.), range of invertebrate taxa, as well as copepod
molts, within the saccate thallus of the red alga Halosaccion glandiforme
Fig. 2 Linear regression analysis of effect of thallus volume on a taxa richness, and b fauna abundance
belonging to 12 taxa in total. Up to 5 taxa and 119 individual invertebrates were found inside one sac. Table 1
also lists the percentage occurrence, mean occurrence, and range of all taxa associated with H. glandiforme.
Nematoda and Arthropoda were the dominant phyla; they made up over 92% of the total fauna. Nematodes
were the most common inhabitants, occurring in 53% of thalli and constituting 70.8% of the total samples.
Although the average number of nematodes per thallus was *10, as many as 107 individuals were found in a
single thallus. Copepods were the second most abundant group, occurring in 30% of thalli and comprising of
21.7% of all species. Nematodes and copepods were found to coexist in 26.1% of the samples. Copepods were
occasionally found in various states of molting. The other lesser represented groups included ostracods,
turbellarians, mites, and bivalves. Numerous copepod nauplii, a few barnacle cyprids, veliger larvae, rotifers,
protozoans, diatoms, crustacean molt remnants, detritus, and sand particles were also found inside thalli.
Results of multiple regression analyses were separated in two groups: (a) thallus volume vs. taxa richness
and abundance, and (b) fluid volume vs. taxa richness and abundance. The thallus volume and the intra-thallus
fluid ranged from 0.42 to 39.27 cm3 (mean 6.02) and 0.1–8.6 mL (mean 1.10), respectively. Overall, larger
thallus volume and greater intra-thallus fluid volume supported higher taxa richness and species abundance.
Taxa richness was positively correlated with thallus volume (F = 4.66, P = 0.03, R2 = 0.05; Fig. 2a) as was
species abundance (F = 10.48, P = 0.002, R2 = 0.11; Fig. 2b). Furthermore, we found positive correlation
between fluid volume and taxa richness (F = 4.25, P = 0.04, R2 = 0.05; Fig. 3a) as well as fauna abundance
(F = 8.75, P = 0.004, R2 = 0.11; Fig. 3b).
A number of feeding interactions between colonizers were noted; they included herbivory, predator–prey
interactions, and detritivory. Most of the invertebrates (e.g., copepods, ostracods, nematodes,
mystacocaridads, rotifers) fed on diatoms and periphyton, some ingested other invertebrates (e.g., flatworm, nematodes,
Fig. 3 Regression analysis of effect of fluid volume on a taxa richness b fauna abundance
copepods, mites), some consumed detritus (ostracods, bivalve, nematodes), and entrapped sediments (mostly
nematodes). Nematodes were also found feeding on bacterial films on the copepod molts, which were common
in our samples (*48% occurrence, with up to 201 molts in a single thallus). As crustacean molts were
common and nematodes are known detritivores (Heip et al. 1985, and references within), it was unsurprising
to find a significant positive relationship between the presence of nematodes and molt remains inside the
thallus (F = 56.77, P \ 0.0001, R2 = 0.40; Fig. 4).
The importance of seaweeds as habitats has been well studied for many rocky intertidal species; however, that
has not been the case for the red alga H. glandiforme. Its fronds are annuals; new thalli appear in late winter
and early spring, but degenerate after spore production during the following fall and winter (Johnson 1994).
With pores as large as 200 lm, microfauna measuring \200 lm most likely enter the fronds via seawater
medium and may leave the hollow sacs either during immersion or when the thalli degenerate at the end of the
growing season. In this novel algal- invertebrate association study, we characterize this seaweed as a
habitatforming species as it shelters multiple invertebrate groups inside its saccate thallus, and provides multiple
benefits for its diverse invertebrate fauna, which in turn, may increase their survivorship and fitness.
Macroalgal traits such as size and morphological complexity can have a large effect on local populations
and communities. The presence of multiple pores on the thallus of H. glandiforme allows seawater into and out
of thalli during tidal cycles and facilitate faunal colonization. Our results show that thallus volume and the
Fig. 4 Relationship between nematode abundance and presence of copepod molts
volume of seawater were important predictors of abundance and richness of invertebrates associated with this
alga. Larger thalli possibly contained more resources, including sea water, which allowed them to shelter
higher numbers of taxa and greater abundance of organisms. It is likely that bigger thalli have larger pores,
which facilitate greater colonization opportunities. These thalli made the coexistence of species with different
ecological necessities possible. Other studies have associated algal morphologies with species diversity and
abundance. When given a choice between Gracilaria vermiculophylla and Ulva rigida, the architecturally
more complex G. vermiculophylla supported higher species richness and diversity of associated macrofauna
(Munari et al. 2015). Steller et al. (2003) also reported that the total organisms supported by rhodoliths,
another group of benthic red alga, significantly increased with branching density and thallus volume.
We found nematodes to be the most abundant group in our samples. This is not surprising since they are
considered to be among the most abundant organisms on earth. Marine roundworms inhabiting high-energy
rocky shores are exposed regularly to changing tidal conditions. Being poor swimmers, they often remain
suspended in the water column before re-entering the benthos as passive particles when tides recede; yet,
nematodes are efficient in choosing algal habitats (Ullberg and O´ lafsson 2003). Nematodes in our algal
samples may have entered the saccate thallus via passive or active mechanisms.
The majority of the nematodes we found belonged to the family Chromadoridae (pers. comm. Ashleigh
Smythe). In a related study at a Brazilian rocky coast, nematode biodiversity was related to the structural
features of macrophyte habitats and the most abundant phytal nematodes were chromadorids (Da Rocha et al.
2006). Chromadorids are often associated with marine macrophytes (Trotter and Webster 1983; Pe´rez-Garc´ıa
et al. 2015). Feeding experiments of the marine nematode Chromadora showed that diatoms and chlorophytes
were preferred food items (Tietjen and Lee 1973). However, Moens and Vincx (1997) reported that many
aquatic nematodes are in fact opportunistic feeders, which may change feeding strategies in response to
available food. We also encountered nematodes belonging to the genus Theristus in our samples. This
freeliving marine nematode group has been found in diverse habitats, including degraded algal beds (Olafsson
et al. 2013) and exposed sandy beaches (Lee and Riveros 2012). Theristus is known to ingest suitably sized
food particles like microalgae cells (Moens and Vincx 1997). Diatoms have been shown to be a prominent
food resource for Theristus (Moens et al. 2014). Diatoms were abundant in our samples and nematodes were
frequently observed ingesting them as well as other items inside the thalli.
We found a positive association between the presences of nematodes and remnants of copepod molts.
Nematodes were observed feeding on the distinct bacterial films covering these molts. As substrate consumers,
nematodes are known to ingest organic substrates along with their associated microflora and microfauna
(Moens et al. 2006). Tietjen and Lee (1973) reported that Chromadora macrolaimoides, isolated from the
collections present on the green alga Ulva intestinalis, consumed different types of bacteria.
Copepods were the second most abundant group in our samples. This too is not unexpected as they are
considered to be one of the most abundant groups in the marine realm. Halosaccion glandiforme belongs to
class Rhodophyceae and, according to Fahrenback (1962), rhodophyceans show higher assemblage of
copepods than other algal groups. Although the exact reasons why red algae are preferred over brown algae
are unknown, Fahrenback (1962) postulates that some red algal fronds are thick enough to accommodate these
crustaceans and prevent their dislodgement. Whereas Fahrenback (1962) observed one harpacticoid copepod
species (Diathrodes cystoecus) in sea sacs collected from Moss Beach, California, we found two genera of
planktonic calanoids, Acartia sp. and Calanus sp. within the algal thalli. They were frequently observed to
feed on diatoms and rotifers, which were plentiful in our samples. As omnivores, they were found to graze
both on phytoplankton (Paffenho¨ fer and Lewis 1989) and protozooplankton (ciliates, heterotrophic
dinoflagellates, flagellates), and rotifers (Stoecker and Egloff 1987).
In addition to serving as feeding grounds, H. glandiforme may also serve as a nursery habitats as gravid
copepods and various larval groups were frequently observed. Copepods were found in various states of
molting, implying their growth and development inside thalli. The presence of other associated taxa suggested
that sea sacs may act as a refuge for multiple species, especially during periods of emersion. According to
Lilley and Schiel (2006), habitat-forming species increases spatial complexity and help ameliorate stressful
environmental conditions, thereby promoting a diversified assemblage of animals. It is obvious that the use of
H. glandiforme as a habitat for invertebrates is multifaceted, as it provides refuge from physical stresses and
predation, facilitates trophic interactions, and serves as nursery ground. As such, this macroalgae should be
addressed in studies dealing with coastal biodiversity conservation.
Acknowledgements We are grateful to A. Smythe for identification of a few taxa. We thank A. Bhaduri for assistance in the field
and two anonymous reviewers for their helpful comments on the manuscript. Laboratory space was provided by the Oregon
Institute of Marine Biology in Charleston, Oregon. This work was funded by California State University Stanislaus Biology
Research Committee and Faculty Development Mini-Grant Awards. The primary author acknowledges the support of A.
Kohlhaas, K. Schoenly, M. Gerson, M. Fleming, P. Kelly, and C. Jantz on this project.
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