et al., 2003). Foraminiferal shells are commonly well preserved in the sedimentary record; they are diverse, relatively small, abundant and easily sampled, and their
collection has minimal impact on environmental resources
(Hallock et al., 2003).
While most Foraminifera are microscopic, adults
of some taxa can be several centimeters in diameter
(Sen Gupta, 2002). Life spans are proportional to size,
ranging from days in small taxa to a few years in very large
ones. The common life cycle in benthic foraminifers
involves alternation of a sexual generation with one
or more asexual generations (Goldstein, 2002; http://
www.ucl.ac.uk/GeolSci/micropal/foram.html). The most
common mode of asexual reproduction is multiple fission,
which can produce broods of tens to hundreds or even
thousands of juveniles, depending upon the volume of
the parent cell. Because meiosis can precede asexual
reproduction, the broods are not necessarily clones.
As early as the seventeenth century, observers of
natural history began noticing the shells and fossils
of the Foraminifera (Sen Gupta, 2002). Antoine van
Leeuwenhoek and Carl von Linné were among the historic
figures who described the complexity of what they
assumed were tiny mollusks. In 1835, Dujardin concluded
that foraminifers were unicellular. Despite observations of
life cycles by Joseph Lister in the late nineteenth century,
far fewer scientists have focused on biological studies of
foraminifers than on fossil successions, distributions
of shells in sediments, and shell geochemistry. Estimates
of extant species range from 3,000 to 5,000, and more than
50,000 fossil species have been described (Pawlowski and
Holzmann, 2008). Yet life cycles of fewer than 30 species
are well documented (Goldstein, 2002). Biological research,
including genetic investigations with the potential to revolutionize foraminiferal systematics, is being conducted in only
a small number of laboratories worldwide.
Historically, the major groups of foraminifers have
been distinguished by wall structure and composition of
the shell, including organic-walled and agglutinated
forms and those that produce calcareous shells (Sen
Gupta, 2002). The calcareous taxa include porcelaneous
imperforate and hyaline perforate shells structures, based
upon crystalline nature and presence or absence of pores.
Loeblich and Tappan (1992) recognized 16 suborders,
which Sen Gupta (2002) elevated to orders based on Lee’s
(1990) elevation of the Order Foraminiferida to Class
Foraminifera. Recent phylogenetic work supports assumptions that the porcelaneous taxa are fundamentally different
from the hyaline taxa, indicating very early evolutionary
divergence of these two lineages (Longet and Pawlowski,
2007).
Organic-walled and agglutinated benthic foraminifers
can be found in most marine environments. However, they
only dominate in environments where calcareous forms
are stressed by reduced saturation of calcium carbonate
such as hyposaline (Figure 2), relatively organic-rich,
and high-latitude or deep-sea environments (Murray,
2006). Agglutinated taxa that secrete calcite cements are
common in more highly saturated environments, including open shelves and coral reefs.
The most important foraminifers associated with environments of normal or near-normal marine salinities,
including coral reefs, are those that produce calcite
(CaCO 3 ) shells (Murray, 2006). Many foraminiferal species use energy to exclude magnesium (Mg) ions during
precipitation of calcite, resulting in shells of a few mole%
of Mg. However, others, including those of the Order
Miliolida that produce porcelaneous shells, precipitate
their shells close to equilibrium with seawater, resulting
in shells that are as much as 13–15 mole% Mg in shallow
tropical waters. Calcite shells containing more than about
8 mole% Mg are relatively soluble when exposed to seawater with reduced carbonate saturation (Morse and
Mackenzie, 1990). Thus, the abundance and diversity of
Miliolida are good indicators of strong carbonate supersaturation. These forms will likely be among the first to
decline as rising atmospheric carbon dioxide concentrations result in progressive ocean acidification (Hallock,
2000).
The other dominant benthic foraminiferal orders that
produce calcite shells are the Rotaliida and the Buliminida
(Sen Gupta, 2002). However, molecular phylogenetic evidence is emerging that this morphological division will
require substantial revision (Longet and Pawlowski,
2007; Schweizer et al., 2008). The Rotaliida include not
only some of the most stress-tolerant generalists, but also
some of the most highly specialized species found among
the Foraminifera (Figure 2). For example, members of the
genus Ammonia are often the last eukaryotes to disappear
from hypoxic or highly polluted habitats (Schafer, 2000).
In contrast, Rotaliida that host algal endosymbionts thrive
and produce vast volumes of carbonate sediments in
extremely nutrient-deficient environments, yet are typically among the first species to decline under anthropogenic pollution (Hallock et al., 2003).
The majority of benthic foraminifers are heterotrophic,
feeding on bacteria, algae, detritus, or combinations thereof.
Feeding strategies include grazers, detritivores, suspension
feeders, herbivores, and carnivores. Some Rotaliida are
kleptoplastic grazers, that is, they can utilize the photosynthetic production from chloroplasts that they harvest from
algae upon which they feed (Goldstein, 2002).
Several families of Miliolida and Rotaliida have
co-evolved with marine algae, diversifying and morphologically specializing to the benefit of their symbiotic relationships (Hallock, 2002; Lee, 2006). The ability of
a holobiont (i.e., host with algal symbionts) to both feed
and photosynthesize is known as mixotrophic nutrition.
This strategy is particularly advantageous in environments
where both dissolved nutrients and particulate food are
relatively scarce, but energy from sunlight is consistently
available, even at quite reduced intensities (Hallock,
2000). Under these conditions, algal symbionts actively
photosynthesize, but because they are severely nutrient
limited, they excrete most of their photosynthetic products
to the host. The host is thereby provided abundant energy
FORAMINIFERA
417
collection has minimal impact on environmental resources
(Hallock et al., 2003).
While most Foraminifera are microscopic, adults
of some taxa can be several centimeters in diameter
(Sen Gupta, 2002). Life spans are proportional to size,
ranging from days in small taxa to a few years in very large
ones. The common life cycle in benthic foraminifers
involves alternation of a sexual generation with one
or more asexual generations (Goldstein, 2002; http://
www.ucl.ac.uk/GeolSci/micropal/foram.html). The most
common mode of asexual reproduction is multiple fission,
which can produce broods of tens to hundreds or even
thousands of juveniles, depending upon the volume of
the parent cell. Because meiosis can precede asexual
reproduction, the broods are not necessarily clones.
As early as the seventeenth century, observers of
natural history began noticing the shells and fossils
of the Foraminifera (Sen Gupta, 2002). Antoine van
Leeuwenhoek and Carl von Linné were among the historic
figures who described the complexity of what they
assumed were tiny mollusks. In 1835, Dujardin concluded
that foraminifers were unicellular. Despite observations of
life cycles by Joseph Lister in the late nineteenth century,
far fewer scientists have focused on biological studies of
foraminifers than on fossil successions, distributions
of shells in sediments, and shell geochemistry. Estimates
of extant species range from 3,000 to 5,000, and more than
50,000 fossil species have been described (Pawlowski and
Holzmann, 2008). Yet life cycles of fewer than 30 species
are well documented (Goldstein, 2002). Biological research,
including genetic investigations with the potential to revolutionize foraminiferal systematics, is being conducted in only
a small number of laboratories worldwide.
Historically, the major groups of foraminifers have
been distinguished by wall structure and composition of
the shell, including organic-walled and agglutinated
forms and those that produce calcareous shells (Sen
Gupta, 2002). The calcareous taxa include porcelaneous
imperforate and hyaline perforate shells structures, based
upon crystalline nature and presence or absence of pores.
Loeblich and Tappan (1992) recognized 16 suborders,
which Sen Gupta (2002) elevated to orders based on Lee’s
(1990) elevation of the Order Foraminiferida to Class
Foraminifera. Recent phylogenetic work supports assumptions that the porcelaneous taxa are fundamentally different
from the hyaline taxa, indicating very early evolutionary
divergence of these two lineages (Longet and Pawlowski,
2007).
Organic-walled and agglutinated benthic foraminifers
can be found in most marine environments. However, they
only dominate in environments where calcareous forms
are stressed by reduced saturation of calcium carbonate
such as hyposaline (Figure 2), relatively organic-rich,
and high-latitude or deep-sea environments (Murray,
2006). Agglutinated taxa that secrete calcite cements are
common in more highly saturated environments, including open shelves and coral reefs.
The most important foraminifers associated with environments of normal or near-normal marine salinities,
including coral reefs, are those that produce calcite
(CaCO 3 ) shells (Murray, 2006). Many foraminiferal species use energy to exclude magnesium (Mg) ions during
precipitation of calcite, resulting in shells of a few mole%
of Mg. However, others, including those of the Order
Miliolida that produce porcelaneous shells, precipitate
their shells close to equilibrium with seawater, resulting
in shells that are as much as 13–15 mole% Mg in shallow
tropical waters. Calcite shells containing more than about
8 mole% Mg are relatively soluble when exposed to seawater with reduced carbonate saturation (Morse and
Mackenzie, 1990). Thus, the abundance and diversity of
Miliolida are good indicators of strong carbonate supersaturation. These forms will likely be among the first to
decline as rising atmospheric carbon dioxide concentrations result in progressive ocean acidification (Hallock,
2000).
The other dominant benthic foraminiferal orders that
produce calcite shells are the Rotaliida and the Buliminida
(Sen Gupta, 2002). However, molecular phylogenetic evidence is emerging that this morphological division will
require substantial revision (Longet and Pawlowski,
2007; Schweizer et al., 2008). The Rotaliida include not
only some of the most stress-tolerant generalists, but also
some of the most highly specialized species found among
the Foraminifera (Figure 2). For example, members of the
genus Ammonia are often the last eukaryotes to disappear
from hypoxic or highly polluted habitats (Schafer, 2000).
In contrast, Rotaliida that host algal endosymbionts thrive
and produce vast volumes of carbonate sediments in
extremely nutrient-deficient environments, yet are typically among the first species to decline under anthropogenic pollution (Hallock et al., 2003).
The majority of benthic foraminifers are heterotrophic,
feeding on bacteria, algae, detritus, or combinations thereof.
Feeding strategies include grazers, detritivores, suspension
feeders, herbivores, and carnivores. Some Rotaliida are
kleptoplastic grazers, that is, they can utilize the photosynthetic production from chloroplasts that they harvest from
algae upon which they feed (Goldstein, 2002).
Several families of Miliolida and Rotaliida have
co-evolved with marine algae, diversifying and morphologically specializing to the benefit of their symbiotic relationships (Hallock, 2002; Lee, 2006). The ability of
a holobiont (i.e., host with algal symbionts) to both feed
and photosynthesize is known as mixotrophic nutrition.
This strategy is particularly advantageous in environments
where both dissolved nutrients and particulate food are
relatively scarce, but energy from sunlight is consistently
available, even at quite reduced intensities (Hallock,
2000). Under these conditions, algal symbionts actively
photosynthesize, but because they are severely nutrient
limited, they excrete most of their photosynthetic products
to the host. The host is thereby provided abundant energy
FORAMINIFERA
417