454
Michael A. Borowitzka, Paul Lavery, and Mike van Keulen
loading (e.g. Silberstein et al., 1986; Tomasko and
Lapointe, 1991; Lapointe et al., 1994), while others have demonstrated shifts in composition of epiphytes under nutrient loading (Wear et al., 1999).
This has led, implicitly, to the assumption that epiphytes could be a useful indicator of environmental
conditions and, in particular, of nutrient concentrations or loads at seagrass sites. However, Lin et al.
(1996) found that nutrient addition (NO 3 , NH 4 , PO 4 ,
either alone or in combination) did not result in
greater epiphyte abundance on Z. marina in their
mesocosms. They argue that this was a result of
their mesocosms containing not only various grazers and omnivorous fish, but also almost all plant
components (seagrasses, seaweeds, phytoplankton,
benthic microalgae, and epiphytes) found in coastal
lagoon ecosystems which competed for light, nutrients, and inorganic carbon. These communities
respond in a complex manner to nutrient addition,
which in turn does not necessarily lead to an increase in the biomass of seagrass epiphytes (see also
Valentine and Duffy, Chapter 20). Lin et al. (loc.
cit.) did, however, observe changes in species composition. In spring, diatoms were dominant in the
controls, PO 4 and NO 3 treatment; whereas green algae and cyanobacteria were dominant in the combined nutrient treatments. In mid-summer the dominant group in the control and PO 4 treatment shifted
to green algae, in the NO 3 treatment the shift was
to cyanobacteria, and in the combined nutrient treatments diatoms dominated. Seasonal influences on
the response of epiphytic algae to nutrient therefore
increases appear to be important. For example, increased epiphyte load on Z. marina due to high nitrogen loading occurred only in summer at Cape Cod,
USA, and coincided with the summer phytoplankton
bloom (Hauxwell et al., 2003).
The literature reviewed in this chapter provides
ample evidence that epiphyte biomass and/or composition responds significantly to nutrient concentration, grazer abundance, hydrodynamic conditions,
depth, and light, and that interactions among these
factors make it difficult to deduce the cause of shifts
in epiphyte biomass or composition. We also reiterate the earliest observations that it is more likely
shifts in both the biomass and the types of epiphytes,
not just the biomass, that can result in seagrass loss.
This proposition was put forward by authors such as
Cambridge et al. (1986) but has become simplified
to the paradigm that it is shifts in epiphyte abundance
alone that cause seagrass loss.
C. Organismal Interactions
1. Grazing and Predation
Seagrass epiphytes are a food source for a range of
grazers and predators and these, in turn, influence
the distribution, diversity, and abundance of the epiphytic organisms. Grazers control epiphytic algal
biomass in at least two ways: directly through the
removal of biomass and indirectly through removal
of host substrate. Grazer–epiphyte interactions have
been reviewed in detail by Jernakoff et al. (1996). It
is abundantly clear from the literature that invertebrate and vertebrate grazers can influence epiphytic
algal abundance (Phillipart, 1995; Alcoverro et al.,
1997; Fong et al., 2000; Heck et al., 2000; Valentine and Duffy, Chapter 20; Heck and Orth, Chapter
22), with estimates that up to 40% of epiphytic algal
production may be lost to grazers (Peduzzi, 1987).
The effect of grazing on epiphyte composition is less
clear, though recent studies do hint at grazing as a
possible structuring force.
Copepods, isopods, and amphipods have been
recorded as significant grazers on seagrass epiphytes, especially the periphyton. For example, they
reduce the accumulation of epiphytic algae on Z.
marina (Duffy et al., 2001), and may also influence
species composition. In microcosm experiments,
Duffy and Harvilicz (2001) showed that seagrass
exposed to grazing by the amphipod Gammarus
mucronatus became overgrown by the red alga
Polysiphonia harveyi compared to ungrazed controls that became heavily fouled with periphyton and
tunicates. In contrast, grazing by the amphithoids
Cymadusa compta and Amphithoe longimana removed virtually all fouling material. Jernakoff and
Nielsen (1997) also noted that grazing by amphipods
appeared to favor crustose coralline algae over
diatoms.
Gastropods consume a wide range of algal epiphytes including the calcareous crustose coralline
algae (Padilla, 1985; Nielsen and Lethbridge, 1989)
and grazing by gastropods also has been shown to
exert a direct control of epiphytic algal biomass on a
wide variety of seagrasses and under a range of conditions (Hootsmans and Vermaat, 1985; Phillipart,
1995; Jernakoff and Nielsen, 1997). However, the release of grazing pressure may provide only a temporary increase in epiphytic algal biomass. Controlled
experiments showed that the absence of grazers results in dramatic increases of epiphytes on Zostera
Michael A. Borowitzka, Paul Lavery, and Mike van Keulen
loading (e.g. Silberstein et al., 1986; Tomasko and
Lapointe, 1991; Lapointe et al., 1994), while others have demonstrated shifts in composition of epiphytes under nutrient loading (Wear et al., 1999).
This has led, implicitly, to the assumption that epiphytes could be a useful indicator of environmental
conditions and, in particular, of nutrient concentrations or loads at seagrass sites. However, Lin et al.
(1996) found that nutrient addition (NO 3 , NH 4 , PO 4 ,
either alone or in combination) did not result in
greater epiphyte abundance on Z. marina in their
mesocosms. They argue that this was a result of
their mesocosms containing not only various grazers and omnivorous fish, but also almost all plant
components (seagrasses, seaweeds, phytoplankton,
benthic microalgae, and epiphytes) found in coastal
lagoon ecosystems which competed for light, nutrients, and inorganic carbon. These communities
respond in a complex manner to nutrient addition,
which in turn does not necessarily lead to an increase in the biomass of seagrass epiphytes (see also
Valentine and Duffy, Chapter 20). Lin et al. (loc.
cit.) did, however, observe changes in species composition. In spring, diatoms were dominant in the
controls, PO 4 and NO 3 treatment; whereas green algae and cyanobacteria were dominant in the combined nutrient treatments. In mid-summer the dominant group in the control and PO 4 treatment shifted
to green algae, in the NO 3 treatment the shift was
to cyanobacteria, and in the combined nutrient treatments diatoms dominated. Seasonal influences on
the response of epiphytic algae to nutrient therefore
increases appear to be important. For example, increased epiphyte load on Z. marina due to high nitrogen loading occurred only in summer at Cape Cod,
USA, and coincided with the summer phytoplankton
bloom (Hauxwell et al., 2003).
The literature reviewed in this chapter provides
ample evidence that epiphyte biomass and/or composition responds significantly to nutrient concentration, grazer abundance, hydrodynamic conditions,
depth, and light, and that interactions among these
factors make it difficult to deduce the cause of shifts
in epiphyte biomass or composition. We also reiterate the earliest observations that it is more likely
shifts in both the biomass and the types of epiphytes,
not just the biomass, that can result in seagrass loss.
This proposition was put forward by authors such as
Cambridge et al. (1986) but has become simplified
to the paradigm that it is shifts in epiphyte abundance
alone that cause seagrass loss.
C. Organismal Interactions
1. Grazing and Predation
Seagrass epiphytes are a food source for a range of
grazers and predators and these, in turn, influence
the distribution, diversity, and abundance of the epiphytic organisms. Grazers control epiphytic algal
biomass in at least two ways: directly through the
removal of biomass and indirectly through removal
of host substrate. Grazer–epiphyte interactions have
been reviewed in detail by Jernakoff et al. (1996). It
is abundantly clear from the literature that invertebrate and vertebrate grazers can influence epiphytic
algal abundance (Phillipart, 1995; Alcoverro et al.,
1997; Fong et al., 2000; Heck et al., 2000; Valentine and Duffy, Chapter 20; Heck and Orth, Chapter
22), with estimates that up to 40% of epiphytic algal
production may be lost to grazers (Peduzzi, 1987).
The effect of grazing on epiphyte composition is less
clear, though recent studies do hint at grazing as a
possible structuring force.
Copepods, isopods, and amphipods have been
recorded as significant grazers on seagrass epiphytes, especially the periphyton. For example, they
reduce the accumulation of epiphytic algae on Z.
marina (Duffy et al., 2001), and may also influence
species composition. In microcosm experiments,
Duffy and Harvilicz (2001) showed that seagrass
exposed to grazing by the amphipod Gammarus
mucronatus became overgrown by the red alga
Polysiphonia harveyi compared to ungrazed controls that became heavily fouled with periphyton and
tunicates. In contrast, grazing by the amphithoids
Cymadusa compta and Amphithoe longimana removed virtually all fouling material. Jernakoff and
Nielsen (1997) also noted that grazing by amphipods
appeared to favor crustose coralline algae over
diatoms.
Gastropods consume a wide range of algal epiphytes including the calcareous crustose coralline
algae (Padilla, 1985; Nielsen and Lethbridge, 1989)
and grazing by gastropods also has been shown to
exert a direct control of epiphytic algal biomass on a
wide variety of seagrasses and under a range of conditions (Hootsmans and Vermaat, 1985; Phillipart,
1995; Jernakoff and Nielsen, 1997). However, the release of grazing pressure may provide only a temporary increase in epiphytic algal biomass. Controlled
experiments showed that the absence of grazers results in dramatic increases of epiphytes on Zostera