480
John F. Valentine and J. Emmett Duffy
of central importance (cf. Hunter and Price 1992;
Hacker and Bertness 1995, 1996). Plant nutritional
quality, often expressed as leaf nitrogen content,
plays a central role in determining the feeding patterns of a diverse array of terrestrial herbivores (e.g.,
Onuf et al. 1977; Slansky and Feeny 1977; Kraft and
Denno 1982; Coley 1983) that preferentially graze
on the leaves of nitrogen-rich plants (e.g. McNeill
and Southwood 1978; Schroeder 1986; Athey and
Connor 1989). By feeding on nitrogen-rich leaves,
herbivores often realize higher survivorship, faster
growth, and higher levels of fecundity (e.g. Feeny
1970; Scriber and Feeny 1977; Rausher 1981; Raupp
and Denno 1983; Schroeder 1986). These findings
have led some investigators to hypothesize that low
leaf nitrogen concentration (not C/N ratio) represents one form of plant defense against grazing by
specialist herbivores (Feeny 1970; Schroeder 1986;
Augner 1995).
Some herbivores, however, have adapted to living
in a world dominated by plants of limited nutritional
content (e.g. McGinnis and Kasting 1967; Mattson
1980; Lincoln et al. 1982; Strong et al. 1984; Slansky and Scriber 1985; Terra et al. 1987; Simpson and
Simpson 1990; Slansky 1993). These adaptations include increasing the length of feeding bouts and/or
increasing rates of consumption to compensate for
shortages in the nitrogen content of the available forage (Mattson 1980; Moran and Hamilton 1980; Price
et al. 1980; Clancy and Feeny 1987). Therefore, low
nutritive value, by itself, is not a universally effective defense against grazing (cf. Boyd and Goodyear
1971; Mattson 1980; Moran and Hamilton 1980).
Compared to the well-studied role of terrestrial
plant nitrogen content on herbivore food selection,
the impact of seagrass leaf nutritional quality (in the
case both leaf nitrogen content and the seeming indigestibility of leaf carbon) in determining food selection in seagrass-dominated ecosystems remains
inadequately investigated. This issue is significant,
given that most marine consumers appear to be broad
generalists, i.e. most feed on a range of primary
producer taxa. Several correlative field studies have
found a significant, positive relationship between
leaf nitrogen content and grazing by vertebrates,
whether parrotfishes, sea turtles, or dugongs (Bjorndal 1980; Zieman et al. 1984; McGlathery 1995;
Preen 1995, but see Cebri´ an and Duarte 1998). There
are no rigorous studies of the importance of diet mixing in determining foraging strategies of seagrassassociated herbivores (e.g. Cruz-Rivera and Hay
2000), despite the domination of marine herbivore
guilds by generalist grazers. Given the diversity of
epiphytic algae in many seagrass beds, it seems likely
that leaf epiphyte composition, which can range from
nutritious diatoms and fleshy green algae to grazerresistant calcareous algae (Klumpp et al. 1993; Heck
et al. 2000), will interact with seagrass leaf nitrogen
content to influence herbivore foraging choices.
As mentioned above very few studies have experimentally investigated the relationship between grazing intensity and nitrogen concentration of seagrass
leaves. Instead studies have relied on comparisons
of published proportional differences in the C/N ratios of seagrass leaves and macroalgae to explain
why herbivores avoid feeding on seagrass leaves
(see Lodge 1991). Yet when detailed comparisons
of absolute nitrogen content are made between algae and vascular macrophytes, the differences tend
to be quite small (Lobel and Ogden 1981; Lowe and
Lawrence 1976; Thayer et al. 1984; Lodge 1991;
Strong 1992; Pillans et al. 2004). So it seems likely
that factors other then the nitrogen content of leaves
are responsible for the relatively low levels of grazing on seagrass leaves. When controlled preference
tests, which include both macroalgae and seagrasses,
have been conducted, seagrass leaves have been
found to be of intermediate palatability in grazer-rich
environments (Hay 1984a). Surprisingly, little consideration has been assigned to what role chemical
feeding deterrents present in these same nitrogenrich macroalgae might make in leading herbivores
to feed on seagrasses. The importance of chemical
deterrents in influencing herbivore food choice are
now well documented in coral-reef and many other
marine ecosystems (e.g. Hay and Steinberg 1992).
Similar studies have not yet been conducted in areas
with high seagrass species richness.
Another intriguing consideration in evaluating
grazing impacts on seagrasses is that some larger
grazers appear capable of managing the nutritional
content of their forage through repetitive grazing.
Using comparisons between grazer exclusion cages
and varying degrees of mechanical simulations of
dugong grazing in nearby open areas, Preen (1995)
inferred that dugongs were cultivating the nutritional condition of their feeding grounds by preventing fibrous, low nitrogen Zostera capricorni from
dominating the submerged landscape. Instead the
disturbance of the sediments by dugong feeding
was hypothesized to allow their preferred forage,
Halophila ovalis, a rapidly growing less fibrous plant
John F. Valentine and J. Emmett Duffy
of central importance (cf. Hunter and Price 1992;
Hacker and Bertness 1995, 1996). Plant nutritional
quality, often expressed as leaf nitrogen content,
plays a central role in determining the feeding patterns of a diverse array of terrestrial herbivores (e.g.,
Onuf et al. 1977; Slansky and Feeny 1977; Kraft and
Denno 1982; Coley 1983) that preferentially graze
on the leaves of nitrogen-rich plants (e.g. McNeill
and Southwood 1978; Schroeder 1986; Athey and
Connor 1989). By feeding on nitrogen-rich leaves,
herbivores often realize higher survivorship, faster
growth, and higher levels of fecundity (e.g. Feeny
1970; Scriber and Feeny 1977; Rausher 1981; Raupp
and Denno 1983; Schroeder 1986). These findings
have led some investigators to hypothesize that low
leaf nitrogen concentration (not C/N ratio) represents one form of plant defense against grazing by
specialist herbivores (Feeny 1970; Schroeder 1986;
Augner 1995).
Some herbivores, however, have adapted to living
in a world dominated by plants of limited nutritional
content (e.g. McGinnis and Kasting 1967; Mattson
1980; Lincoln et al. 1982; Strong et al. 1984; Slansky and Scriber 1985; Terra et al. 1987; Simpson and
Simpson 1990; Slansky 1993). These adaptations include increasing the length of feeding bouts and/or
increasing rates of consumption to compensate for
shortages in the nitrogen content of the available forage (Mattson 1980; Moran and Hamilton 1980; Price
et al. 1980; Clancy and Feeny 1987). Therefore, low
nutritive value, by itself, is not a universally effective defense against grazing (cf. Boyd and Goodyear
1971; Mattson 1980; Moran and Hamilton 1980).
Compared to the well-studied role of terrestrial
plant nitrogen content on herbivore food selection,
the impact of seagrass leaf nutritional quality (in the
case both leaf nitrogen content and the seeming indigestibility of leaf carbon) in determining food selection in seagrass-dominated ecosystems remains
inadequately investigated. This issue is significant,
given that most marine consumers appear to be broad
generalists, i.e. most feed on a range of primary
producer taxa. Several correlative field studies have
found a significant, positive relationship between
leaf nitrogen content and grazing by vertebrates,
whether parrotfishes, sea turtles, or dugongs (Bjorndal 1980; Zieman et al. 1984; McGlathery 1995;
Preen 1995, but see Cebri´ an and Duarte 1998). There
are no rigorous studies of the importance of diet mixing in determining foraging strategies of seagrassassociated herbivores (e.g. Cruz-Rivera and Hay
2000), despite the domination of marine herbivore
guilds by generalist grazers. Given the diversity of
epiphytic algae in many seagrass beds, it seems likely
that leaf epiphyte composition, which can range from
nutritious diatoms and fleshy green algae to grazerresistant calcareous algae (Klumpp et al. 1993; Heck
et al. 2000), will interact with seagrass leaf nitrogen
content to influence herbivore foraging choices.
As mentioned above very few studies have experimentally investigated the relationship between grazing intensity and nitrogen concentration of seagrass
leaves. Instead studies have relied on comparisons
of published proportional differences in the C/N ratios of seagrass leaves and macroalgae to explain
why herbivores avoid feeding on seagrass leaves
(see Lodge 1991). Yet when detailed comparisons
of absolute nitrogen content are made between algae and vascular macrophytes, the differences tend
to be quite small (Lobel and Ogden 1981; Lowe and
Lawrence 1976; Thayer et al. 1984; Lodge 1991;
Strong 1992; Pillans et al. 2004). So it seems likely
that factors other then the nitrogen content of leaves
are responsible for the relatively low levels of grazing on seagrass leaves. When controlled preference
tests, which include both macroalgae and seagrasses,
have been conducted, seagrass leaves have been
found to be of intermediate palatability in grazer-rich
environments (Hay 1984a). Surprisingly, little consideration has been assigned to what role chemical
feeding deterrents present in these same nitrogenrich macroalgae might make in leading herbivores
to feed on seagrasses. The importance of chemical
deterrents in influencing herbivore food choice are
now well documented in coral-reef and many other
marine ecosystems (e.g. Hay and Steinberg 1992).
Similar studies have not yet been conducted in areas
with high seagrass species richness.
Another intriguing consideration in evaluating
grazing impacts on seagrasses is that some larger
grazers appear capable of managing the nutritional
content of their forage through repetitive grazing.
Using comparisons between grazer exclusion cages
and varying degrees of mechanical simulations of
dugong grazing in nearby open areas, Preen (1995)
inferred that dugongs were cultivating the nutritional condition of their feeding grounds by preventing fibrous, low nitrogen Zostera capricorni from
dominating the submerged landscape. Instead the
disturbance of the sediments by dugong feeding
was hypothesized to allow their preferred forage,
Halophila ovalis, a rapidly growing less fibrous plant