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MICROSCOPY RESEARCH AND TECHNIQUE 37:116–135 (1997)
Epibiotic Microorganisms on Copepods
and Other Marine Crustaceans
KEVIN R. CARMAN1* AND FRED C. DOBBS2
1Department
2Department
of Zoology and Physiology, Louisiana State University, Baton Rouge, Louisiana 70803-1725
of Oceanography, Old Dominion University, Norfolk, Virginia 23529-0276
KEY WORDS:
epibiosis; symbiosis; algae; diatoms; fungi; protozoa; bacteria; Vibrio; review
ABSTRACT
Although the occurrence of microbial (algal, protozoan, bacterial, and fungal)
epibionts on marine crustaceans and other invertebrates has been documented repeatedly, the
ecological context and significance of these relationships generally are not well understood.
Recently, several studies have examined the population and community ecology of algal and
protozoan epibionts on freshwater crustaceans. Even so, the study of microbial epibionts in aquatic
environments is still in its infancy. In this review, we summarize associations of microalgae,
protozoans, and bacteria with marine crustaceans, especially copepods. We note differences and
commonalities across epibiont taxa, consider host-epibiont cycling of nutrients, generate hypotheses
relevant to the ecology of the host and the epibiont, and suggest future research opportunities.
Microsc. Res. Tech. 37:116–135, 1997. r 1997 Wiley-Liss, Inc.
The presence or absence of microorganisms epibiotic on
animals may play an important role in the life of the
animal. It seems logical that an adequate description of
the epibiotic microbiota, at least that on the smaller forms,
should become an integral part of the description and
study of marine animals.
Sieburth (1975)
INTRODUCTION
It has long been recognized that aquatic microorganisms (algae, protozoans, bacteria, and fungi) in general,
and bacteria in particular, have a strong affinity for
surfaces (e.g., Cooksey and Wigglesworth-Cooksey, 1995;
Costerton et al., 1978; Zobell, 1943). It is more recently
evident that surfaces of many, if not most, limnetic,
estuarine, and marine metazoans are suitable sites for
attachment and growth of epibiotic microorganisms.
Indeed, Sieburth (1975) listed the ‘‘epibiotic’’ (literally,
‘‘living on’’) environment as one of five major microbial
environments in aquatic systems. He noted that ‘‘animal surfaces . . . especially the chitinous skeleton of
crustaceans, appear to be nutrient surfaces that encourage bacterial attachment and growth and undergo
extensive colonization.’’ The crustacean component of
these associations is variously referred to as the substrate organism, the host, or the basibiont (Wahl, 1989).
A larger list of descriptive terms is applied to the
microorganisms involved, including ectocommensal,
ectosymbiont, epicuticular, epifauna, episymbiont, epizoan, epizoic (and the variant spelling epizooic), epizoite, and microflora. While our choice is to use the
words epibiont and epibiotic, we consider all these
terms to be legitimate. We argue, however, that whatever term is used, it should not suggest a functional
relationship (e.g., mutualist, commensal, or parasite)
without evidence of such. When we use the term
symbiosis, we mean it in the broadest of contexts (i.e.,
living together).
Although the occurrence of microbial epibionts on
marine crustaceans and other invertebrates has been
r 1997 WILEY-LISS, INC.
documented repeatedly, in general, the ecological context and significance of these relationships are not well
understood; papers by Fenchel (1965) and Weissman et
al. (1993) represent notable exceptions. In this review,
we report and summarize various microbial associations with marine crustaceans, especially copepods. We
complement, expand, and update an overview of copepod symbionts (Ho and Perkins, 1985). We note
differences and commonalities across epibiont and host
taxa, consider host-epibiont cycling of nutrients, generate hypotheses relevant to the benefits and costs of the
host and epibiont, and offer suggestions for research
opportunities.
It is useful to delineate what this paper does not
encompass. First, we did not consider epibionts other
than those on the crustacean exoskeleton. Arguably,
microorganisms on the branchial chambers, the gill
filaments, or even on the gut lining, chitinized or not,
may be considered to be ‘‘epibiotic,’’ as they are outside
the animal in a histological sense. Second, we only once
appraised epibionts on crustacean eggs, although such
associations may be very important with respect to
infection sequences and density-dependent regulation
of crustacean populations (e.g., Shields, 1994). Third,
we chose only to reference, not to incorporate, informative reviews of epibionts on crustaceans grown in
aquaculture operations (e.g., Brock and LeaMaster,
1992; Lightner, 1983; Sindermann, 1990). Fourth, we
rarely focused on epibionts associated with freshwater
crustaceans, as their algal and protozoan epibionts
recently have been a focus of research (e.g., Allen et al.,
1993; Gaiser and Bachmann, 1994; Threlkeld et al.,
1993). While generally not discussing freshwater forms,
*Correspondence to: Kevin R. Carman, Department of Zoology and Physiology,
Louisiana State University, Baton Rouge, LA 70803-1725.
Received 25 March 1995; Accepted in revised form 14 June 1995
MICROBIAL EPIBIONTS ON MARINE CRUSTACEANS
we have gleaned considerable ecological insight from
freshwater researchers.
To continue, we cover algal, protozoan, and bacterial
epibionts of marine crustaceans in this review. A fourth
major category of microorganisms, the Fungi, presented little to synthesize. First, most information
about fungal symbionts is in the aquaculture-disease
literature and was outside our purview. Second, nearly
all crustacean-associated fungi develop in the host’s
cuticle or in its underlying soft tissue; thus, the fungi
are not epi- but endobiotic. Third, fungi that might be
considered truly epibiotic are found not on crustacean
carapaces but are saprophytic on crustacean eggs, a
habitat we consider only once. Finally, given that
research with pathogenic forms has been emphasized,
we know of very little effort to study less benign
fungal-crustacean associations. Reviews of fungal diseases of Crustacea (Johnson, 1983; Unestam, 1973) and
a recapitulation of their relevant sections (Ho and
Perkins, 1985) describe epidemics, some causing profound mortality, in zooplankton. Additional information
about mycoses is available in aquacultural reviews
listed above.
We begin by separately reviewing associations of
algae, protozoans, and bacteria on crustaceans. The
sections covering algae and protozoans follow a different format from that used for bacteria, reflective of the
profound differences in approaches to studying these
different microbial taxa. In the final section of the
paper, however, we consider commonalities and differences among these several groups of epibionts.
STUDY SITES AND METHODS
Although much of the information in this review is
from the literature, significant amounts of material,
including all electron microscopy images, are from our
previously unpublished studies. Our specimens were
obtained from four sites. Labidocera sp. was collected
from surface water at a eutrophic site in the northern
Gulf of Mexico off the coast of Louisiana (within the
plume of the Mississippi River) (Carman, 1994). Palaemonetes pugio, Coullana sp., and Pseudostenhelia wellsi
were collected from saltmarsh mudflats near the Louisiana Universities Marine Consortium facility in Cocodrie, LA. Zausodes arenicolus and Heteropsyllus nunni
were collected from an intertidal sandflat near the
Florida State University Marine Laboratory (Carman
and Thistle, 1985). Robertsonia sp. was collected from
shallow (1 m water depth) patch reefs in Kaneohe Bay,
Oahu, Hawaii (Caetta and Dobbs, 1990).
Specimens were preserved and processed for scanning electron microscopy as detailed by Felgenhauer
(1987). In essence, glutaraldehyde-fixed copepods were
dehydrated in a graded series of ethanol, critical-pointdried, mounted on stubs, and coated with gold/palladium. Specimens were examined using a variety of
scanning electron microscopes (see Acknowledgments);
details are available from the authors. For transmission electron microscopy (TEM), specimens were fixed
with 4% glutaraldehyde in 0.1 M sodium cacodylate
buffer with 0.35 M sucrose, decalcified with EDTA in
fixative, rinsed in buffer, postfixed with 1% OsO4, and
dehydrated in a graded ethanol series. Specimens were
embedded in LX112, and ultrathin sections were double-
117
stained with uranyl acetate and lead citrate and then
examined in a Zeiss 10/A electron microscope.
ALGAL EPIBIONTS
The term algal is used here in a very broad sense and
includes photoautotrophic microorganisms that arguably are protozoans or cyanobacteria. Diatoms, however, account overwhelmingly for the reports of microalgae on marine crustaceans. The apparent dominance of
diatoms as epibionts, relative to other algal types, may
indeed be the case in marine systems, but we suggest
that there is a bias favoring the detection and recognition of these comparatively large, geometrically distinct, silicified forms over smaller, less widely recognized organisms.
Diatoms on Copepods
Hiromi et al. (1985) summarized a variety of reports
concerning diatoms epibiotic on marine copepods (e.g.,
Gibson, 1978, 1979; Hiromi and Takano, 1983; Jurilj,
1957; Russell and Norris, 1971; Simonsen, 1970). Although about twenty species of epibiotic diatoms have
been reported, Hiromi et al. (1985) evaluated the
considerable taxonomic confusion involved, determined
that there was much synonymy, and concluded that
only five diatom species, representing the families
Protoraphidaceae and Diatomaceae, are significantly
involved in episymbiosis with marine copepods.
There is some level of host-symbiont specificity;
particular diatoms apparently consort only with certain
copepod hosts (Hiromi et al., 1985; Prasad et al., 1989).
The most widespread and abundant of these diatoms
are Pseudohimantidium pacificum, found principally
on corycaeid copepods, and Protoraphis atlantica, associated mainly with pontellid and candacid copepods
(Hiromi et al., 1985). Although calanoid and cyclopoid
copepods have been most commonly reported as having
diatom epibionts, harpacticoid copepods, both pelagic
(Gibson, 1978, 1979; Hiromi and Takano, 1983) and
benthic (Carman, 1989), also serve as substrates.
In general, diatoms attach to the copepod’s exoskeleton using stalks or pads (Fig. 1A–D). Both are mucilaginous secretions, with the distinction being in the length
of the attachment structure; pads are shorter (Hoagland et al., 1993). In contrast to such attachments, one
of us (K.R.C.) has found diatoms having prostrate
attachments (Hoagland et al., 1993) to the exoskeleton
of Coullana sp., a harpacticoid copepod formerly referred to as Scottolana canadensis in literature from
Louisiana studies (Fig. 1E). Morphologies of such diatoms are typical of epipelic forms (Round, 1971).
Russell and Norris (1971) found that attachment
sites of Pseudohimantidium pacificum varied systematically between male and female copepods, with a much
higher abundance of diatoms on the second antennae of
males and on the carapace and thoracic segments of
females. While males had diatoms on their genital and
anal segments, Russell and Norris (1971) considered
that ‘‘spermatophores and egg masses in these areas
probably interfere(d) with diatom attachment’’ to females. From these assessments, they proposed that
diatoms were transferred during ‘‘copulatory or noncopulatory clasping’’ of the copepods. Gibson (1978,
1979) concurred and expanded on the premise that
distribution patterns of Pseudohimantidium pacificum
118
K.R. CARMAN AND F.C. DOBBS
Fig. 1. Epibiotic diatoms on marine copepods. A: Colony of diatoms
near the genital pore of a calanoid copepod, Labidocera sp. Bar 5 50
µm. B: Higher magnification of cell-cell articulation indicated by
arrow b in A. Bar 5 1 µm. C: Higher magnification of attachment to
copepod surface indicated by arrow c in A. Bar 5 5 µm. D: Stalked
diatoms attached in the urosome-mesosome intersegmental region of
Labidocera sp. Bar 5 50 µm. E: Naviculoid diatoms with prostrate
attachment on the dorsal surface of the urosome of Coullana sp. Bar 5
20 µm.
MICROBIAL EPIBIONTS ON MARINE CRUSTACEANS
and Protoraphis atlantica on copepods are related to
the hosts’ mating behavior. Patterns were more specific
on calanoids than on harpacticoids, presumably a result of the different mating habits of these two groups.
On the other hand, Hiromi and Takano (1983) and
Hiromi et al. (1985) reported the opposite result; distributions of diatoms were more discrete on harpacticoid
than on calanoid copepods.
There is little information concerning the abundance
of diatoms on marine copepods, and the range is great.
Russell and Norris (1971) reported seven to nine cells
individual21 of Pseudohimantidium pacificum on Corycaeus affinis. Gibson (1979) considered Labidocera aestiva to be ‘‘heavily infested’’ when it harbored .1,000
cells of Protoraphis atlantica individual21. Even this
seemingly high value is small compared to a freshwater
association in which the cladoceran Daphnia harbored
up to 2.3 3 104 diatoms (Synedra cyclopum) individual21 (Allen et al., 1993). Fewer data exist concerning the incidence of epibiotic diatoms on copepods. The
only population-level study is that of Russell and Norris
(1971), who found up to 55–82% of a population of
Corycaeus affinis to have Pseudohimantidium pacificum as epibionts.
Diatoms on Other Crustaceans
Few reports exist of diatoms epibiotic on marine
crustaceans other than copepods. Sieburth (1975) presented scanning electron micrographs of diatoms Licmophora, Cocconeis, and Synedra on the body of an
amphipod, Caprella grahamii. McClatchie et al. (1990)
found that up to 50–70% of a euphasiid population,
Nyctiphanes australis, harbored high abundances of
epibiotic diatoms (Licmophora sp.). The researchers’
concern was that the chlorophyll content of the epibionts might introduce a source of error into copepod
grazing rates based on gut fluorescence or radioisotopes. Indeed, heavily infested individuals yielded results that overestimated their actual grazing rates by a
factor of two to five.
Other Algae
In their discussion of the diatom, Pseudohimantidium pacificum, living on the copepod, Corycaeus
affinis, Russell and Norris (1971) reported a ‘‘brown
algal filament’’ and ‘‘isolated brown algal cells’’ as other
epibionts. They gave no further information.
Møhlenberg and Kaas (1990) reported an infestation
of Colacium vesiculosum, a freshwater euglenoid, on
four species of calanoids (Acartia sp., Centropages
hamatus, Temora longicornis, and Pseudocalanus elongatus). Some copepods had algal cell densities sufficient
to register fluorescent pigment values 25 times greater
than uninfested individuals. (The above-mentioned concern of McClatchie et al. (1990) with respect to grazing
rates certainly would apply in this case!) That a ‘‘freshwater’’ euglenoid was involved was thought to be related to low salinity, high temperature, and large
numbers of copepods.
Shelton (1974) described a filamentous cyanobacterium, up to 240 µm in length, living on field and
laboratory populations of an estuarine shrimp, Crangon crangon. The filaments were located on the shrimps’
chemoreceptor setae, but Shelton tested for and found
no evidence of impaired chemoreception. A congeneric
119
but truly marine shrimp, C. allmani, harbored no
cyanobacteria. Epibiotic cyanobacteria are common in
freshwater crustaceans, but we know of only one other
report for their occurrence on marine crustaceans, a
gammarid amphipod (Fenchel, 1965).
Discussion
Although diatoms appear to be the dominant microalgae on marine copepods and other crustaceans, we
again caution that a sampling bias may favor their
discovery and reporting. In low-salinity waters, reports
by Shelton (1974) and Møhlenberg and Kaas (1990)
suggest that microalgae other than diatoms may prevail as photoautotrophic epibionts of crustaceans.
Previous investigators have considered the ecological
significance of marine copepod-diatom associations.
The most informative references (Gibson, 1979; Hiromi
et al., 1985; Ikeda, 1977; Russell and Norris, 1971)
collectively review previous marine literature, observations, and speculations concerning the effects of the
epibionts on the copepods’ swimming, respiration, and
mating success. In addition, Ikeda (1977) and Gibson
(1979) considered the potential nutritional benefits
accrued by the epibionts. Here we synthesize these
particulars and contribute our own thoughts. These
ideas may well be applied to other microbial epibionts,
and, indeed, we will subsequently refer back to these
points. Given the relatively large size of diatoms,
however, we predict that any size-related effects of
epibionts on their host will be more pronounced with
diatoms than with fungi, protozoans, or bacteria.
Klevenhusen (1933, cited in Russell and Norris,
1971) first suggested that epibiotic diatoms might
increase the buoyancy of copepods, presumably lessening energy requirements for swimming. While this idea
has been echoed repeatedly, we know of no experiments
testing the hypothesis. In the opposite sense, Russell
and Morris (1971) suggested that diatoms might hinder
the action of the copepods’ swimming legs. Gibson
(1979) mentioned that it was unknown whether swimming speed was affected by epibionts. Were such the
case, however, then the potential for predation on the
host certainly would certainly increase, as has been
suggested in freshwater studies (e.g., Willey et al.,
1990). Furthermore, diatoms may not only negatively
affect swimming speed but increase the host’s visibility
to predators (see Willey et al., 1993, and references
therein).
Physiological studies seem well suited to provide
insight into short-term, nonlethal ramifications of epibiont loads on copepods. We know of only one study,
however, in which diatom-infested, marine copepods
were tested. Ikeda (1977) used animals so heavily
infested they appeared to be ‘‘covered with rags’’ and
found no significant differences in respiration rate or
excretion of ammonia and inorganic phosphate relative
to noninfested copepods. In a freshwater study, Allen et
al. (1993) also found no difference in respiration rates
between diatom-infested and diatom-free cladocerans,
Daphnia. There was an increased mortality of diatominfested hosts, however, and Allen et al. (1993) considered physiological stress to be the causative factor. We
are unaware of any marine copepod-feeding studies in
which diatom epibionts have been noted, much less
considered as a variable, but if gut-fluorescence meth-
120
K.R. CARMAN AND F.C. DOBBS
ods are to be used, investigators should keep in mind
the potential for overestimation of grazing rates (McClatchie et al., 1990).
Ikeda (1977) suggested that epibiotic diatoms would
encounter ‘‘rich nutrients just excreted’’ by their hosts.
Without being specific about a mechanism, Gibson
(1979) wrote of the benefit of a ‘‘moving host continually
replenishing (the diatoms’) nutrient supply.’’ Indeed, we
presume that through excretion the host copepod provides to its diatom epibionts a heightened availability
of nutrients and dissolved organic matter (DOM). Copepods also release nutrients and DOM into the surrounding water during so-called ‘‘sloppy feeding’’ (Conover,
1966; Dagg, 1974). In moving to areas in which concentrations of its own food are greater, the copepod would
transport diatom epibionts to the enriched environment. Finally, the host’s swimming would result in a
thinner, hydrodynamic-boundary layer about itself, thus
facilitating the diffusion of dissolved constituents from
the ambient water to epibiotic diatoms.
The idea of nutrient provision to epibiotic diatoms
seems to be well grounded conceptually. It is intriguing,
therefore, to recall the only pertinent data; Ikeda (1977)
found no difference in the excretion of ammonia and
inorganic phosphate between copepods heavily infested
and not infested with diatoms. If the epibionts were
indeed sequestering nutrients excreted by their hosts,
then an infestation-related difference presumably would
have emerged.
With respect to nutrient transfer from diatom to
copepod, there is no record of hosts feeding on algae
attached to their exoskeleton. Trophic level transfers of
much greater importance concern predation on the
host-symbiont association. Gibson (1979) did not know
‘‘whether predators . . . make use of the additional
energy and nutrient supply afforded by the attached
diatoms.’’
In concluding their review article, Hiromi et al.
(1985) wondered why ‘‘epizoic diatoms seem to attach
exclusively to pelagic copepods.’’ In fact, such diatoms
occur on Coullana sp., a harpacticoid copepod with a
semiplanktonic lifestyle (Fig. 1E). Therefore, epibiosis
is not associated absolutely with pelagic copepods. It
may be significant, however, that we have not observed
diatoms on Pseudostenhelia nunni, a benthic harpacticoid that cooccurs in Louisiana with Coullana sp.
Among several individuals of various harpacticoids
(Zausodes arenicolus, Halicyclops coulli, Heteropsyllus
nunni, Leptastacus constrictus) from a Florida sandflat,
we detected stalked diatoms on only one individual of
H. nunni. Furthermore, we have not found epibiotic
diatoms on benthic copepods from Hawaii. This general
phenomenon may occur simply because diatoms associated with benthic copepods may not be well exposed to
light. Indeed, Coullana lives in sediment burrows and
makes excursions into the water column only at night
(Decho, 1986; Radziejewska, personal communication),
as do many other benthic copepods (Walters, 1991).
Thus, it is not apparent that epibiotic diatoms on
Coullana would gain any advantage in terms of exposure to light. Their presence on the copepod, then, must
involve another factor(s), which we presume is related
to provision of nutrients from host to epibiont.
PROTOZOAN EPIBIONTS
Protozoan epibionts of crustaceans appear to be
predominantly members of the phylum Ciliophora, of
the subclasses Hypostomata, Suctoria, Hymenostomata, Peritricha, and Spirotricha (Corliss, 1979; classification follows that of Corliss, 1979). To a lesser extent,
other groups of protozoans reported as epibiotic on
crustaceans include foraminiferans, naked rhizopods,
and choanoflagellates. Ellobiopsids also have been reported as epibionts, and, given that they have for
decades eluded successful phylogenetic classification,
we simply follow the lead of earlier researchers (e.g.,
Johnson, 1983) and include them here.
Protozoans on Copepods
Among ciliophorans, members of the subclasses Suctoria and Peritricha have been most widely reported as
epibionts on marine copepods (Table 1). Their levels of
infestation vary from 0–100% of the individuals in the
copepod populations under study. In general, however,
it seems that low levels of infestation either are unnoticed or unreported. The number of epibionts per copepod ranges over two orders of magnitude: 1–20
(Marshall and Orr, 1955); 25–200 (Herman and Mihursky, 1964); 1–250 (Sherman and Schaner, 1965); 1–2
(Humes and Ho, 1968); 1–50 (Herman et al., 1971);
1–80 (Sieburth et al., 1976); 1–8 (Bowman, 1977); and
0–160 (Weissman et al., 1993).
Infestation sometimes is specific for the copepod’s sex
(Marshall and Orr, 1955) or developmental stage
(Conover, 1956; Marshall and Orr, 1955; Turner et al.,
1979); at other times neither factor applies (sex: Herman and Mihursky, 1964; developmental stage: Herman and Mihursky, 1964; Herman et al., 1971; Weissman et al., 1993). Some researchers have concluded
that infestation may be more predictably related to the
relative sizes of the copepod host and the ciliate epibiont than to other factors (Herman et al., 1971; Sherman
and Schaner, 1965; Weissman et al., 1993).
Some protozoan epibionts locate themselves specifically on certain parts of the copepod, (e.g., Ophyrodendron sp. on the caudal ramus of Lichomolgus singularipes [Humes and Ho, 1968]). Sieburth et al. (1976)
found suctorians ‘‘in a band along the waterline’’ of
surface-dwelling pontellid copepods. Other epibionts
attach in a more catholic manner (e.g., Weissman et al.
(1993) reported Rhabdostyla on all sides of the cephalothorax and on the urosome of Acartia hudsonica).
In the three studies that report long-term ($1 year)
data, infestation was strongly seasonal (Nagasawa,
1988; Sherman and Schaner, 1965; Weissman et al.,
1993). In the latter two studies, the presence of the
epibionts was strongly correlated with the seasonal
presence of the copepods. Such correlation is consonant
with the high level of specificity epibionts exhibit for
the host; other cooccurring copepods rarely carry ciliates that heavily infest the principal host (Herman and
Mihursky, 1964; Nagasawa, 1988; Sherman and
Schaner, 1965; Turner et al., 1979).
In addition to the subclasses Suctoria and Peritricha,
apostome ciliates (subclass Hypostomata) have long
been known to be epibionts on copepods (e.g., Chatton
and Lwoff, 1935) and range in their symbiotic relation-
121
MICROBIAL EPIBIONTS ON MARINE CRUSTACEANS
TABLE 1. Ciliophorans epibiotic on marine copepods1
Subclass
Peritricha
Taxon/Taxa
Rhabdostyla sp.
Epistylus sp.
Zoothamnium sp.
Zoothamnium alterans
Zoothamium sp.
Vorticella sp.
Myoschiston centropagidarum
Cothurnia sp. (recurva?)
Vaginicolidae
Suctoria
Ephelota gemmipara
Paracineta sp.
Thecacineta inclusa, T. cothurnoides
Lecanophrya sp.
Hypostomata
Dendrosomides lucicutiae
Ophryodendron sp.
Vampyrophrya pelagica
Vampyrophyra pelagica, Gymnodinoides sp.
Hymenostomata
1See
Uronema sp.
Copepod
Reference
Acartia hudsonica
Acartia tonsa
Acartia tonsa, A. clausi
Acartia tonsa
Centropages abdominalis, Acartia
omorii
Corycaeus affinis
Eurytemora affinis, Acartia tonsa
Paronychocamptus curticaudatus,
Esola typhlops
Stenocaris pygmea, Ameira parvula
Scottolana, Amphiascus, Typhlamphiascus, Orthopsyllus, Enhydrosoma
Pontella scutifer
Metridia
Stenocaris pygmea, Cylindropsyllus
laevis, Evansula incerta, Paraleptastacus espinulatus, Amphiascoides nanus, Heterolaophonte littoralis
Parathalestris intermedia, Nitocra
spinipes
Lucicutia gaussae, L. flavicornis
Lichomolgus singularipes
Centropages hamatus, C. typicus,
Acartia tonsa, A. longiremis, Corycaeus sp., Eurytemora sp., Labidocera aestiva, Eucalanus sp., Paracalanus sp., Oncaea minuta
Parathalestris intermedia, Rhynchothalestris rufocincta, Paramphiascopsis longirostris, Pseudonychocamptus proximus, Heterolaophonte
minuta
Huntemannia jadensis
Weissman et al., 1993
Turner et al., 1979
Herman and Mihursky, 1964
Sieburth et al., 1976
Nagasawa, 1986a
Russell and Norris, 1971
Hirche, 1974
Hockin, 1984
Herman et al., 1971
Sieburth et al., 1976
Sherman and Schaner, 1965
Hockin, 1984
Hockin, 1984
Bowman, 1977
Humes and Ho, 1968
Grimes and Bradbury, 1992
Hockin, 1984
Hockin, 1984
Sherman and Schaner (1965, their Table 1) for a summary of earlier reports.
ship from exuviotrophic ectocommensals to parasites
(Bradbury, 1994; Grimes and Bradbury, 1992). Despite
their complex life cycles and difficulties in their identification (based upon the morphology of their feeding
stage, the vegetative trophont), the apostomes’ interactions with copepods are comparatively well understood
in some cases. In particular, histophagous species may
be found encysted on appendages of their hosts. Should
the copepod be injured or ingested by an invertebrate
predator, the apostomes excyst and the trophonts utilize the copepod’s soft tissues for nutrition. Once fed,
the apostomes encyst and divide, and the next generation swims forth seeking copepods. The histophage
Vampyrophrya pelagica, found on at least seven genera
of copepods (Table 1), has been well studied in this
regard (Grimes and Bradbury, 1992). Although a second
host is not required for Vampyrophyra to complete its
life cycle, the second host (a predator of copepods)
benefits the apostome either by injuring the copepod
and initiating the single-host life cycle or by killing and
ingesting the copepod, continuing the two-host life cycle
(Grimes and Bradbury, 1992). Hockin (1984) noted that
only surface-dwelling or epiphytic benthic copepods
were infested with apostomes, not interstitial ones. He
considered this point potentially important for the
ciliophorans’ completion of their life history via the
second host; that is, he considered predation a less
likely fate for interstitial copepods. Additional information on this intriguing group of ciliophorans is found in
Bradbury (1994).
In addition to ciliophoran epibionts, we report here
finding choanoflagellates on Coullana sp., a marine
harpacticoid copepod cultured by Prof. Darcy Lonsdale
(Fig. 2C). It seems reasonable to assume that many
other kinds of flagellates are epibiotic on copepods but
are unreported as yet.
Finally, whether they are protozoans or not, three
species of ellobiopsids (genus Ellobiopsis) have been
reported from many species of pelagic marine copepods
(Table 1 in Shields, 1994). Flagellated spores of Ellobiopsis settle onto setae of their host’s buccal appendages.
There they metamorphose into trophomeres and extrude a root-like organelle through the copepod’s cuticle, presumably to absorb nutrients (Shields, 1994).
Penetration causes at least localized damage to host
exoskeleton and underlying muscle; in addition, infection may reduce fecundity or even cause parasitic
castration (Shields, 1994). Typically, only one or two
trophomeres mature simultaneously, but each parasite
may have a volume up to 7.5% that of its host; Wickstead (1963) hypothesized that the parasites’ nutritional demands might cause the host to starve. Given
its location on the host, Ellobiopsis may also utilize food
particles not ingested by the copepod. Additional details
about Ellobiopsis biology are related by Marshall and
Orr (1955), Ho and Perkins (1985), and Shields (1994).
Protozoans on Other Crustaceans
In their annotated inventory of ciliate epibionts on
decapods, Sprague and Couch (1971) listed 23 (possibly
122
K.R. CARMAN AND F.C. DOBBS
Fig. 2. Epibiotic protozoa on marine crustaceans. A: Peritrich
ciliate Lagenophrys sp. completely covering the surface of a Palaemonetes pugio egg. Bar 5 100 µm. B: Higher magnification of a Lagenophrys sp. individual. Bar 5 20 µm. C: Epibiotic choanoflagellate on
Coullana sp. Bar 5 1 µm.
24) genera of epibiotic ciliates distributed among ten
families across four orders: Holotrichia, Peritrichia,
Spirotrichia, and Suctoria (classification follows that of
their paper). This tally does not include protozoans
living in the branchial chambers or on the gill filaments
of their hosts.
The peritrich genus Lagenophyrs comprised an intriguing component of their inventory; its speciation
was particularly compelling. Sprague and Couch (1971)
listed 52 species within the genus, 22 of which exhibited
strong host specificity within the Decapoda. Subsequently, Felgenhauer (1982) reported Lagenophrys as
an epibiont on a variety of marine and freshwater
decapods belonging to the infraorders Anomura,
Brachyura, Astacidea, and Caridea. Depending upon
the host species, the ciliates are frequently associated
with gill lamellae but may be specifically associated
with appendages or generally distributed over the
exoskeleton of the decapod. One of us (K.R.C.) has
observed Lagenophrys sp. on the eggs of Palaemonetes
pugio (Fig. 2A,B).
More recently, Camacho and Chinchilla (1989) published a taxonomic key to ciliates epibiotic on natant
decapods, listing 13 genera distributed among ten
families. In a subsequent paper, they demonstrated
that seven of these ciliate genera are not randomly
distributed on the freshwater shrimp, Macrobrachium
rosenbergii, but are positioned in a manner that maximizes the feeding efficiency exhibited by the different
protozoans and partitions the resources made available
by the host (Granados and Chinchilla, 1990).
Other reports are less diverse taxonomically. Euphausiids harbor populations of ciliophorans (McClatchie
et al., 1990, and references therein); in particular, an
ecological study of Euphausia superba by RakusaSuszczewski and Filcek (1988) provides much pertinent
information. Three species of protozoans that attach to
the appendages of the krill were examined over time.
The three species exhibited site-specific attachment (or
at least site-specific proliferation). More than 99% of
the krill population was infested, and the degree of
infestation was greater in autumn than in spring. From
this and their other studies, the researchers suggested
that the species composition of the protozoan epibionts
might provide a clue to the geographical origin of the
krill population.
Jones and Khan (1970) found a ciliate, Conidophrys
sp. (cf. pilisuctor), attached to the antennules, antennae, and peraeopods of males and females of the isopod
Jaera albifrons. Their literature review indicated that
this epibiont also occurs on Corophium, Erichthonius,
Microdeutopus, two species of Jassa, two species of
Gammarus, and Dexamine (amphipods) as well as on
Limnoria and Idotea (isopods). The epibiont’s congener,
C. guttipotor, is found on Sphaeroma (isopod).
In landmark ecological research, Fenchel (1965) studied 25 ciliophoran species associated with five marine
species of the amphipod Gammarus. He showed that
the distribution of many epibionts was site-specific on
the host and classified the epibionts into four feeding
groups (suspension feeders, herbivores, carnivores, and
parasites). He demonstrated that peritrichs and chonotrichs formed swarming cells in anticipation of their
host’s molting. He judged 18 ciliates to be epibionts
specific to the genus, found no ciliates in common
MICROBIAL EPIBIONTS ON MARINE CRUSTACEANS
between freshwater and saltwater gammarids, and
determined that the greatest number of ciliate species
was associated with brackish-water populations of the
amphipods. Fenchel’s detailed study, published over 30
years ago, presaged some of current ecological interest
in these associations (e.g., Fenchel, 1987).
Ciliophorans certainly are the dominant protozoans
on crustaceans, but other phyla within the Protozoa
have been reported as well. Smaldon (1974) found a
foraminiferan, Neoconorbina sp., on the carapace of a
porcelain crab, Pisidia longicornis. Moore (1985) described foraminiferans, Cibicides lobatulus, on the isopod Astacilla longicornis. Although females were host
to more foraminiferans than males, Moore believed
that size, hence, length of the intermolt period, was the
critical factor in determining the level of infestation.
His subsequent examination of museum material revealed another foraminiferan, Miliolinella subrotunda,
as well as naked agglutinating rhizopods on other
specimens of A. longicornis.
Finally, members of the taxonomically enigmatic
Ellobiopsidae have been reported as epibionts on euphausiids, amphipods, mysids, carideans, and decapods (e.g., Johnson, 1983; Shields, 1994; Vader, 1973).
The range of epibiont-host relationships is great. For
example, although the life cycle and attachment sites of
Ellobiocystis are thought to be similar to Ellobiopsis
(see previous section), the former do not penetrate the
body of their hosts, principally shrimps and mysids,
and Shields (1994) classifies them as commensals. On
the other hand, members of the genus Thalassomyces
infect a variety of crustaceans and are overtly parasitic.
However, the externally visible symptoms of such infection are trophomeres extruded through the host’s cuticle following internal development of the parasite
(Shields, 1994); thus, Thalassomyces is not an epibiont
in a strict sense.
Discussion
While there has been speculation for decades about
the potential effects of protozoan epibionts on their
hosts (and vice versa), experimental approaches have
only recently been attempted. Fenchel’s (1987) statement is telling: ‘‘Colonial peritrichs are very common on
planktonic copepods, so much so that they could have a
significant ecological impact, but this has never been
studied.’’ Since then, the freshwater literature has seen
a plethora of pertinent publications. The marine literature, by comparison, is paltry. For example, the May
1993 issue of Limnology and Oceanography contained
six articles dealing with algal and protozoan epibionts
on zooplankton, only one of which dealt with a marine
copepod (Weissman et al., 1993).
From the viewpoint of population ecology, the most
elegant work on marine copepod-epibiont interactions
is that of Weissman et al. (1993), who studied infestation of Acartia hudsonica by the peritrich Rhabdostyla
sp. They showed that egg production but not hatching
success was negatively correlated with the number of
epibionts per copepod. Peritrich-infested nauplii had
lower rates of survival, but their developmental rates
were not affected. The possible population-level ramifications of these effects are intriguing.
Weissman et al. (1993) also demonstrated that live
copepods bearing epibionts sank significantly slower
123
than uninfested copepods. Their results are opposite
those of Herman and Mihursky (1964), who used preserved copepods and determined sinking rates 100–300
times greater. Weissman et al. (1993) proposed that
increased drag associated with ciliate infestation creates a ‘‘parachutelike effect.’’ It is not clear, however,
whether sinking rates may be extended to swimming
rates (i.e., the speed necessary to escape from a predator). Thus, infestation may or may not be disadvantageous to the copepod host with respect to swimming
speed. The increased visibility of a highly infested host,
however, may result in increased predation, as has been
suggested (Willey et al., 1990) and experimentally
demonstrated (Willey et al., 1993) in freshwater studies.
Another potentially negative effect of the epibiont on
its host was suggested by Turner et al. (1979), who
found lesions attractive to bacteria at sites where the
peritrich, Epistylis, attached to the copepod, Acartia
tonsa. The presence of epibiotic bacteria suggested to
them microbial utilization of dissolved organic matter
(DOM). They hypothesized that attachment of ciliophorans, and the copepods’ subsequent loss of internal body
contents, may influence the seasonal change in populations of estuarine copepods. This idea was echoed by
Nagasawa (1986a, 1988), who showed bacteria attached to former attachment sites of protozoan epibionts. Thus, provision of DOM and other nutrients to
protozoan epibionts may occur not only via excretion,
feeding, and transport phenomena, as suggested earlier
for attached diatoms, but also through leakage from a
histologically compromised carapace.
BACTERIAL EPIBIONTS
Our review’s format changes with this section on
bacteria. First, very nearly all the literature dealing
with these microorganisms as symbionts on crustaceans concerns copepods. Thus, there is no organizational gain in segregating the relatively few reports
that cover other crustacean taxa. Second, despite a
decrease in size of the individual epibiont, when bacteria are abundant on copepods, their metabolic impact
on the surrounding water may be biogeochemically
profound. Third, and as a consequence of the second,
researchers’ questions and approaches differ slightly to
substantially from those applied to algal and protozoan
epibionts.
Incidence and Abundance
Table 2 lists reports of epibiotic bacteria on aquatic
crustaceans; most involve microscopical studies of bacterial epibionts. A few (Carli et al., 1993; Davis and
Sizemore, 1982; Gil-Turnes et al., 1989; Huq et al.,
1984; Sochard et al., 1979) involve the use of cultural
techniques. Only two studies deal with freshwater
crustaceans (Holland and Hergenrader, 1981; Nagasawa, 1988), reflecting the greater interest shown by
marine researchers in copepod-bacterial associations.
Nagasawa has been a prolific contributor to the
literature and in her review (Nagasawa, 1989) found
that the ‘‘incidence of copepods with bacteria’’ (ICWB)
from all available reports varied from 0–100%. Nagasawa (1986b) reported that ICWB was unrelated to
the abundance of free-living bacteria and suggested
that bacterial colonization of copepods may involve the
124
K.R. CARMAN AND F.C. DOBBS
TABLE 2. Reports of epibiotic bacteria on crustaceans1
Host
Copepods
Diaptomus sp., D. nevadensis
Acartia clausi
A. longiremis, A. tonsa, A. spp.
A. omerii, A. plumosa
A. clausi
Pseudocalanus minutus
Calanus cristatus
Acartia tonsa
Labidocera aestiva
Pontellopsis regalis
Pleuromamma sp.
Centropages furcatus
Tigriopus fulvus
Copepods
Halicyclops coulli, Zausodes
arenicolus, Robertsonia sp.
Robertsonia sp.
Labidocera sp.
Coullana sp.
Pseudostenhelia wellsi
Porcellidium
Decapods
Various decapods
Callinectes sapidus
Paleamon macrodactylus
Homarus americanus
Pagurus longicarpus
Planes minutus
Carcinus maenus
C. irroratus, Lithodes maio, H.
americanus
Palaemonetes pugio
Other crustacea
Caprella grahamii (amphipod)
Jassa falcata (amphipod)
Limnoria tripunctata (isopod)
Boeckosimus afinis (amphipod)
Limnoria tripunctata, L.
lignorum (isopods), and Chelura terebrans (amphipod)
L. lignorum
Epibiont
Pseudomonas, Bacillus, Acinetobacter, Flavobacterium
Bacteria
Bacteria
Bacteria
Bacteria
Bacteria
Bacteria
Vibrio, Chromobacterium, Pseudomonas, Cytophaga, or Flavobacterium
Vibrio, Pseudomonas, Cytophaga,
or Flavobacterium
Pseudomonas, Vibrio
Pseudomonas
Vibrio, Pseudomonas
V. alginolytus, Aeromonas spp.,
Pseudomonas spp.
V. cholerae, V. parahaemolyticus
Bacteria, rods, filamentous
Location
Appendages, genital opening,
joints
Joints, legs, depressions
Antennule, ventral side, legs,
labrum, body
Everywhere
Depressions, antennules
Antennae, mandible
Joints, mandible, urosome
Reference
Holland and Hergenrader, 1981
Nagasawa et al., 1985
Nagasawa, 1986a
Nagasawa, 1986b
Nagasawa and Terazaki, 1987
Sochard et al., 1979
Egg sac, body
Carli et al., 1993
Egg sacs, mouth, body
Legs, mouth, joints
Huq et al., 1983, 1984
Carman, 1990
Bacteria, rods, filamentous, cocci
Legs, mouth, joints, anus
Bacteria, rods, filaments; diatoms
Bacteria, filaments, rods; diatoms
Bacteria, rods
Bacteria
Legs, mouth, joints, anus
Legs, mouth, joints, anus
Legs, mouth, joints
Pits on dorsal surface of body
Caetta and Dobbs (1990); this
study
This study
This study
This study
Gharagozlou-Van Ginneken and
Bouligand, 1975
Leucothrix
Antennules, gills, embryos, carapace, eyes, cephalic region, legs,
joints
Bauer, 1989a
Vibrio cholerae, V. vulnificus, V.
parahaemolyticus
Alteromonas sp.
Leucothrix mucor
L. mucor
L. mucor
L. mucor
L. mucor
Davis and Sizemore, 1982
Embryos
Body, appendages
Antennae
Pleopods
Antennae, pleopods
Eggs
L. mucor
Pleopods, eggs
Filamentous bacteria
Bacteria
Bacteria: rods, cocci, stalked
None detected
Bacteria, rods
Body
Body
Mouth parts, legs, telson
Pleopods and pleotelson
Sleeter et al., 1978
Atlas et al., 1982
Boyle and Mitchell, 1978
Aeromonas hydrophila, Pseudomonas, Vibrio
Pleopods and pleotelson
Boyle and Mitchell, 1981
Gil-Turnes et al., 1989
Sieburth, 1975
Johnson et al., 1971
Sieburth, 1975
1See also Nagasawa (1989) for further listings. When only bacteria is listed as the epibiont, the bacterial taxa were not determined. Where bacterial names are given,
they are not necessarily comprehensive but represent those species that were identified. Bacterial morphologies, when reported, are also noted.
physiological activity or developmental stage of the
host. Carli et al. (1993), however, noted that Vibrio
alginolyticus abundance on the copepod Tigriopus fulvus was positively correlated to the abundance of V.
alginolyticus in the water but did not consider the
possible importance of copepod developmental stage.
Copepods shed their carapace (and any associated
epibionts) at the transition between each naupliar and
copepodite stage and do not molt again after adulthood.
Thus, bacterial (and other) epibionts are more likely to
accumulate on copepods after the terminal molt has
occurred. As such, copepod populations consisting primarily of copepodites should contain relatively fewer
epibionts than populations consisting primarily of
adults.
Epibiotic bacteria have been routinely observed on a
variety of crustaceans other than copepods, including
isopods, amphipods, and decapods (Table 2). These
reports, however, have been largely anecdotal. For
example, large accumulations of epibiotic bacteria on
isopods and amphipods have been reported from studies designed to examine gut bacteria (Boyle and Mitchell,
1978). Atlas et al. (1982) noted that no epibiotic bacteria
could be found on the benthic Arctic amphipod Boeckosimus affinis. Intriguingly, however, other cooccurring
amphipod species had ‘‘extensive’’ (Atlas et al., 1982)
MICROBIAL EPIBIONTS ON MARINE CRUSTACEANS
assemblages of epibiotic bacteria. The reason(s) for this
dramatic difference in epibiotic bacteria on cooccurring
amphipod species is not known.
Also listed in Table 2 are the locations on the host at
which bacterial epibionts were reported to be most
abundant. This compilation of anecdotal information
may be of use in future studies. For example, as
discussed below, different Vibrio species show different
distribution patterns on copepods. In general, many
hosts have epibiotic bacteria that accumulate around
the anus, in intersegmental regions, and near mouth
parts. These bacteria apparently proliferate in areas
where excretion or leakage of organic and inorganic
nutrients are greatest; presumably they exploit these
resources. Other hosts, however, are characterized by
more even distributions of bacteria. Perhaps these
latter bacteria merely use the host as a generic site for
attachment. It would be interesting to understand the
basis for variability in epibiotic bacterial distribution
on different host species.
Although some investigations have failed to detect
epibiotic bacteria, we feel that it is difficult to demonstrate the definitive absence of bacteria, especially in
light of their uneven and cryptic distribution. As discussed below, these distribution patterns also have
implications for determining the abundance of epibiotic
bacteria.
Presumably because of the technical difficulties associated with their quantification, only a few investigators have even offered an estimate of the abundance of
epibiotic bacteria on crustaceans. Nagasawa (1986c)
estimated that adult Acartia (planktonic copepods) had
10–105 epibiotic bacteria. Holland and Hergenrader
(1981) estimated epibiotic bacterial abundance on freshwater copepods to be approximately 6 3 105 bacteria
per copepod. These estimates were based on scanning
electron microscopy (SEM) examination of copepods,
but neither Holland and Hergenrader (1981) nor Nagasawa (1986c) provided details of how counts were
determined. As noted above, epibiotic bacteria on copepods are generally not evenly distributed over the
exoskeleton but are concentrated in particular areas
(e.g., Boyle and Mitchell, 1978; Carman, 1990), such as
between segments (Fig. 3A,B), around mouthparts (Fig.
3C,D), near the anus (Fig. 3E–I), and on legs (Fig. 3J).
Epibiotic bacteria are also frequently present in dense
clumps (Fig. 3K), which would be virtually impossible
to enumerate unless the clumps were somehow dispersed. Thus, the uneven distribution of epibiotic bacteria makes their quantification with SEM extremely
problematic. Further, epibiotic bacteria may be cryptic
and not detectable by routine SEM examination. For
example, TEM examination of copepod sections (Fig.
3L) and SEM examination of copepods that have had
legs and mouth parts removed (Fig. 3M,N) show that
epibiotic bacteria are frequently hidden from view.
Finally, although many epibiotic bacteria appear to
adhere strongly to crustacean surfaces, no attempt has
been made to determine the number of bacteria lost as
the result of preparing specimens for SEM examination.
Based on their determination of colony-forming units
(CFU), Sochard et al. (1979) concluded that ‘‘many more
bacteria were found associated with copepods than
were found to be free-living in the water column,’’ but
125
the absolute amounts of bacteria associated with copepods were not specified. It is also not clear how possible
biases of the culturing techniques used could have
influenced comparisons between abundances of freeliving vs. epibiotic bacteria. Boyle and Mitchell (1981)
used acridine-orange direct counts to estimate that
approximately 1.4 3 107 epibiotic bacteria per individual were present on the wood-boring isopod Limnoria lignorum. They also noted that plate counts consistently yielded approximately 100 times fewer bacteria
(i.e., 105 ) per isopod. Carli et al. (1993) detected as
many as 105 CFU associated with the rockpool harpacticoid copepod Tigriopus fulvus but did not attempt to
perform direct counts for comparison. If Carli et al.’s
(1993) cultural techniques yielded underestimates of
bacterial abundance comparable to those reported by
Boyle and Mitchell (1981), the copepods would appear
to harbor approximately as many epibiotic bacteria as
the much larger Limnoria.
Host Specificity: Vibrios
Members of the bacterial genus Vibrio seem to have a
particularly strong affinity for surfaces, especially under nutrient-limiting conditions (Dawson et al., 1981).
Indeed, Hood et al. (1984) noted that the preferred
habitat of V. cholerae is ‘‘the epibiotic one in which it
lives attached to the substrate.’’ The evidence cited
below indicates that vibrios are especially fond of
crustacean surfaces. Vibrio harveyi, for example, possesses specific proteins for attachment to chitin (Montgomery and Kirchman, 1993, 1994), but the generality
of this attachment mechanism has not been determined. Vibrios have also been shown to possess chitinolytic enzymes and thus may be able to use crustacean
exoskeletons as a growth substrate (Bassler et al.,
1991). Bacterial degradation of living crustacean exoskeletons has been demonstrated for copepods (Nagasawa, 1987) (Fig. 4), but the identify of these chitindegrading bacteria has not been determined. Bacterial
degradation of decapod exoskeleton (e.g., ‘‘shell disease’’) is a commonly associated with various Vibrio
spp., especially among animals reared in aquaculture
facilities (Sindermann, 1990). Montgomery and Kirchman (1993) demonstrated that enzymes involved in
chitin degradation are distinct from proteins involved
in attachment to chitin.
Even though certain bacteria such as vibrios show an
affinity for surfaces, there is little evidence that specific
relationships exist between crustacean hosts and their
bacterial epibionts. The available indications, however,
suggest that the epibiotic bacterial assemblage associated with zooplankton is taxonomically distinct from
free-living bacteria. Sochard et al. (1979) used culture
techniques to characterize and quantify the bacterial
assemblage associated with Acartia tonsa. They found a
diverse assemblage of bacteria associated with healthy
copepods. These bacteria were primarily associated
with external surfaces of copepods and were dominated
by members of the genus Vibrio. A. tonsa collected from
an estuarine environment (Chesapeake Bay) had a
higher incidence of vibrios than either pelagic or laboratory-reared A. tonsa.
Huq et al. (1983, 1984), also using culture techniques,
found that V. cholerae and V. parahaemolyticus preferentially attach to planktonic copepods relative to other
126
K.R. CARMAN AND F.C. DOBBS
Fig. 3A–F. Epibiotic bacteria on marine crustaceans. A: Colony of
rod-shaped bacteria with prostate attachment on dorsal mesosome of
Pseudostenhelia wellsi (harpacticoid copepod). Note plaque that has
formed at intersegmental articulation. Bar 5 20 µm. B: Dense growth
of rod-shaped bacteria around the pereopod articulation with the body
of a planktonic amphipod. Bar 5 50 µm. C: Ventral view of Zausodes
arenicolus (harpacticoid copepod) showing feeding appendages. Bar 5
20 µm. D: Magnified view of region indicated by arrow in C showing
colony of rod-shaped bacteria with polar attachment. Bar 5 1 µm. E–I:
Epibiotic bacteria associated with the caudal region of copepods.
E: Filamentous bacteria on the terminal urosome segment on Robertsonia sp. (harpacticoid). Bar 5 10 µm. F: Higher magnification of
filaments shown in E. Note that rod-shaped bacteria with a polar
attachment have densely colonized the surface of the filamentous
bacteria. Bar 5 1 µm.
MICROBIAL EPIBIONTS ON MARINE CRUSTACEANS
Fig. 3G–L. G: Caudal rami of Labidocera sp. (calanoid). Bar 5 100
µm. H: Magnified view of region designated by the arrow in G; a colony
of rod-shaped bacteria with polar attachment is seen. Bar 5 10 µm.
I: Rod-shaped bacteria with prostate attachment on the caudal rami of
Robertsonia sp. Bar 5 10 µm. J: Rod-shaped bacteria with polar
attachment on the P1 exopod of Zausodes arenicolus. Bar 5 1 µm.
127
K: Rod-shaped bacteria with prostate attachment growing on ventral
surface of planktonic amphipod. In the upper left corner of the panel, a
large clump of bacteria is attached to the amphipod surface. Bar 5 50
µm. L: TEM image of bacteria attached to cryptic regions around the
mouth of Coullana sp. Arrows point to bracketed regions where
bacteria were detected. Bar 5 10 µm.
128
K.R. CARMAN AND F.C. DOBBS
Fig. 3M,N. M: Filamentous bacteria growing cryptically around the mouth region of Labidocera sp.
These filaments were detected only after feeding appendages were dissected from the copepod. Bar 5 10
µm. N: A higher magnification showing cryptic filamentous bacteria attached to copepod exoskeleton.
Bar 5 5 µm.
Fig. 4. Bacterial degradation of copepod exoskeleton. Regions
resembling craters are associated with the site of the polar attachment
of these rod-shaped bacteria on Labidocera sp. Bar 5 1 µm.
bacteria (e.g., E. coli and Pseudomonas sp.) and suggested that copepods serve as a reservoir for pathogenic
species such as V. cholerae O1. This relationship led
Huq et al. (1984) to suggest that there was a ‘‘correlation between incidence of planktonic copepods and the
distribution of V. cholerae.’’ They also observed in
laboratory studies that the presence of live copepods
stimulated V. cholerae to grow from densities of 104
ml21 to 108 ml21; when bacteria were incubated with
dead instead of live copepods, bacterial abundance
increased to only 106 ml21. Live (or dead) copepods did
not stimulate similar growth by other bacterial species
tested (V. parahaemolyticus or Pseudomonas sp.). Further, Huq et al. (1984) showed that V. cholerae readily
attached to copepods and that the attached cells were
particularly concentrated in the oral region and on egg
sacs of copepods. Very little attachment to copepods was
observed for E. coli or Pseudomonas sp. V. parahaemolyticus attached to copepods but was distributed evenly
over copepod surfaces and not concentrated in particu-
lar areas. It is not known if the lateral attachment of V.
parahaemolyticus vs. the polar attachment of V. cholerae (Belas and Colwell, 1982) influences a differential
spatial distribution on copepods. Huq et al. (1984)
suggested that association of V. cholerae with the oral
region and eggs of copepods could both lead to effective
means of dispersal; eggs released by copepods would
carry with them an inoculum for copepod nauplii when
they hatch, and bacteria associated with the oral region
could be ingested during normal feeding and dispersed
in fecal pellets. Given the apparent strong affinity of V.
cholerae for copepods, Huq et al. (1984) suggested that
seasonal variability in V. cholerae abundance may be
closely linked with variability in the abundance of
copepods.
The different distributions of V. parahaemolyticus
and V. cholerae on copepods observed by Huq et al.
(1984) may also reflect different nutritional requirements. If V. cholerae is stimulated by copepod exudates,
then living around the oral region would provide an
optimal proximity to material released from ‘‘sloppy
feeding’’ (see discussion of algal epibionts) as well as to
excretions of liquid waste through the maxillary pores.
V. parahaemolyticus, which is apparently not stimulated by copepod exudates, may simply use copepods as
a surface for attachment, and thus their attachment
sites are nonspecific. It would also be interesting to
contrast these Vibrio species in terms of their ability to
degrade chitin. If V. cholerae derives its nutrition from
living copepods, one might predict that it would attach
to copepod surfaces but not degrade the exoskeleton. V.
parahaemolyticus, which does not seem to be stimulated by copepod exudates, may exploit the nutrients
available in the copepod exoskeleton.
Kaneko and Colwell (1973, 1975) presented evidence
that V. parahaemolyticus overwintered in sediment and
then attached to the exterior surfaces of zooplankton
where they proliferated. They noted that more than
80% of the environmental isolates of V. parahaemolyticus were from zooplankton dominated by copepods.
Huq et al. (1990) used fluorescent antibodies (FA) to
detect V. cholerae O1 in Bangladesh waters. V. cholerae
MICROBIAL EPIBIONTS ON MARINE CRUSTACEANS
O1 were detected in 64% of plankton samples, whereas
cultural methods led to the detection of V. cholerae O1
in only 0.3% of plankton samples. V. cholerae O1 was
detected on zooplankton with FA, and its occurrence
was ‘‘most extensive’’ (Huq et al., 1990) on copepods.
These observations compelled Huq et al. (1990) to
suggest that V. cholerae attach to plankton to withstand
environmental shifts in temperature, salinity, or nutrients and during this period were nonculturable and
thus undetectable by conventional microbiological techniques. Dietrich et al. (1984) also speculated that V.
cholerae may attach to the surface of the blue crab
Callinectes sapidus as a survival mechanism.
Carli et al. (1993) examined the relationship between
the copepod Tigriopus fulvus and Vibrio alginolyticus in
tide pools. Using cultural techniques for quantification,
they noted a strong affinity of V. alginolyticus for T.
fulvus in general and for egg sacs in particular. The
abundance of V. alginolyticus on T. fulvus, however,
appeared to be a direct response to the abundance of V.
alginolyticus in water, and thus the relationship appears to be opportunistic. Boyle and Mitchell (1981)
also detected V. alginolyticus (and other Vibrio spp.) on
the wood-boring isopod Limnoria lignorum.
Thus, there is a substantial body of literature that
links the ecology of various Vibrio spp. with that of
crustaceans in general and copepods in particular.
Much of this evidence is, however, strictly correlative or
inferred from laboratory studies. Some field observations, however, do not support the hypothesis that the
ecology of all vibrios is closely linked to zooplankton (or
other crustaceans). Venkateswaran et al. (1989) serotyped environmental isolates from Japanese coastal
waters and detected no seasonal relationship between
V. cholerae and zooplankton. Further, although Tamplin et al. (1990) found that V. cholerae preferentially
attached to live vs. dead copepods in the laboratory,
they were unable to detect V. cholerae associated with
zooplankton collected from Bangladesh waters. Clearly,
more work is needed to understand the significance of
species-specific relationships between bacteria and crustaceans.
Host Specificity: Nonvibrios
The rationale for studying Vibrio clearly has its basis
in public-health microbiology. From the standpoint of
pure microbial ecology, it would be good to understand
the association of other bacterial types with their
crustaceans hosts. For example, micrometer-scale diversity along the spermatophore of a harpacticoid copepod
is illustrated in Figure 5A–D, in which a variety of
bacterial morphologies is distributed along a gradient
extending approximately 90 µm. How many bacterial
species are include in this assemblage? How are the
species interacting with one another (i.e., do they
compete for limiting resources)? What is the level of
host specificity, if any?
In one of the few studies of epibiotic bacteria not
focused on pathogenic vibrios, Boyle and Mitchell (1981)
found that the most abundant bacterium living on the
exoskeleton of Limnoria lignorum was Aeromonas hydrophila, which is, intriguingly, another known pathogen to humans and other vertebrates. Venkateswaran
et al. (1989) noted that several serotypes of Salmonella
sp. appeared to be found exclusively on zooplankton in
the coastal waters of Japan.
129
The occurrence of the filamentous bacterium Leucothrix mucor is reported to be ‘‘widespread on benthic
crustacea’’ (Johnson et al., 1971). L. mucor can also be
found on algae, other invertebrates, and nonorganismal
surfaces (Sieburth, 1975). Thus, while L. mucor may
have an affinity for crustacean surfaces, its occurrence
is certainly not limited to crustaceans.
Size of Epibiotic Bacteria
Bacteria attached to particles or aggregates such as
marine snow tend to be larger than free-living bacteria
(e.g., Iriberri et al., 1987; Simon, 1987). Alldredge and
Gotschalk (1990) found that the average bacterial cell
volume on various types of marine snow ranged from
0.11–0.21 µm3, which was greater than that of freeliving bacteria by a factor of 1.1–1.9. Similarly, Iriberri
et al. (1987) found that attached bacteria (0.102 µm3
cell21 ) were about twice as large as free-living bacteria
(0.047 µm3 cell21 ). The volumes of epibiotic bacteria on
copepods examined in this study were determined from
SEM micrographs. Rods on benthic copepods
(0.177 6 0.124 µm3 cell21; mean 6 1 s.d.) were larger
than those on planktonic copepods (Labidocera sp.;
0.125 6 0.069 µm3 cell21 ) but not significantly so. Cell
biovolumes of filamentous epibiotic bacteria were fiveto tenfold higher than those of rod-shaped epibiotic
bacteria, and filamentous bacteria on benthic copepods
(1.189 6 0.432 µm3 cell21 ) were significantly larger
than those on Labidocera sp. (0.501 6 0.167 µm3 cell21 ).
Overall, the biovolumes of epibiotic bacteria (this
study) are considerably larger than biovolumes of freeliving or attached bacteria (e.g., Alldredge and
Gotschalk, 1990; Iriberri et al., 1987). The differences
in size may in fact be somewhat underestimated, as
Fuhrman (1981) suggested that cell volumes determined with SEM are significantly less than those
determined using acridine-orange staining (the method
commonly used in the above-cited references). Larger
bacteria are generally considered to be an indication of
nutritionally favorable conditions (Morita, 1982). Our
data indicate that epibiotic bacteria are considerably
larger than free-living bacteria or bacteria associated
with nonliving aggregates. As discussed below, we
hypothesize that the larger size of these bacteria is a
consequence of the nutritionally favorable conditions
that they experience.
Metabolic Relationships
There is at least anecdotal evidence that epibiotic
bacteria associated with crustaceans are metabolically
quite active (Anderson and Stephens, 1969; Carman,
1989, 1990). Enhanced activity by epibiotic bacteria has
also been reported for bacteria associated with the
external surfaces of hydrothermal-vent invertebrates
(de Angelis et al., 1991). Boyle and Mitchell (1981)
suggested that epibiotic bacteria on Limnoria could
exploit organic carbon and inorganic nitrogen released
by the isopods.
As noted above, planktonic bacteria attached to nonliving particles are frequently larger and/or have higher
metabolic rates than free-living bacteria. The contribution of attached bacteria to overall bacterial production,
activity, or biomass, however, is highly variable (range
0–100%; see literature review by Iriberri et al. [1987]).
In a broad sense, zooplankton could be considered as a
form of ‘‘suspended (non-sinking) particulate material,’’
130
K.R. CARMAN AND F.C. DOBBS
Fig. 5. Diversity of epibiotic bacteria. A: A gradient of bacterial
morphologies is found associated with a spermatophore attached to a
female Robertsonia sp. Bar 5 10 µm. B: At one end of the spermatophore (designated by arrow b in A), large cocci predominate. Bar 5 5
µm. C: Small filamentous forms become relatively more abundant in
the region designated by arrow c in A. Bar 5 5 µm. D: At the opposite
end (arrow d in A), the small filamentous forms are numerically
dominant, and a colony of large filaments is present. Bar 5 5 µm.
Karl et al. (1988) with which a large fraction of bacterial activity may be associated. Many water-column
procedures for studying microbial activity, however,
include pre- or postscreening through mesh to eliminate larger animals (e.g., Chin-Leo and Kirchman,
1990; Karl et al., 1988; Kirchman and Mitchell, 1982;
Simon, 1987). Prescreening would remove from consideration any effects of epibiotic bacteria, and postscreening would sequester those effects with the trapped
invertebrates. In any case, explicit investigations of
activity by bacteria associated with the surfaces of
marine invertebrates are lacking.
Jumars et al. (1989) proposed that byproducts of
grazing are the principal mechanisms by which dissolved organic carbon (DOC) is transferred to bacteria,
and many authors have noted that bacterial activity
and production is enhanced in the presence of copepods
(e.g., Carman, 1994; Copping and Lorenzen, 1980;
Eppley et al., 1981; Mopper and Lindroth, 1982; Peduzzi
and Herndl, 1992). In addition to DOC, crustaceans
excrete large and relatively constant quantities of
NH41 (e.g., Gardner and Paffenhöfer, 1982) that may
provide an important source of N for marine bacteria
(Wheeler and Kirchman, 1986).
As an alternative strategy to their association with
fecal pellets, bacteria might better exploit nutrients
liberated by zooplankton by maintaining themselves in
close spatial proximity to the grazer. As opposed to the
ephemeral and finite resources available from fecal
pellets, grazers would represent a continuous source
(i.e., a ‘‘sustained gradient’’ [Azam and Ammerman,
1984]) of nutrition for bacteria that would persist for
many bacterial generation times. Relatively fast swimming speeds of zooplankton, however, would prevent
motile bacteria from efficiently exploiting microzones of
enhanced nutrients that surround zooplankton (Jackson, 1987; Purcell, 1977). Alternatively, bacteria could
exploit zooplankton exudates by becoming physically
attached to grazers. The distribution of bacteria on both
planktonic and benthic copepods is consistent with this
hypothesis. Bacteria are typically abundant in the anal
region (Fig. 3E–I) and around mouth parts (Fig. 3C,D)
and intersegmental areas (Fig. 3A) where release of
nutrients should be highest.
Carman (1994) has determined that, at an abundance of 0.1 copepod ml21, epibiotic bacteria on Labidocera sp. account for approximately 20% of the total
bacterial activity in surface-water samples from the
MICROBIAL EPIBIONTS ON MARINE CRUSTACEANS
Gulf of Mexico. Further, Carman concluded that liberation of amino acids and NH41 by Labidocera significantly stimulated activity by free-living bacteria.
Collectively, the available information indicates that
bacteria-crustacean interactions could be significant to
the ‘‘microbial loop’’ and biogeochemical cycles in general. These relationships undoubtedly vary spatially
and temporally in association with events such as
phytoplankton blooms and zooplankton (e.g., euphasiids) swarms.
Effects on Substrate Organism
The evolutionary significance of epibiotic microbes is
well illustrated by the fact that many decapod (Bauer,
1989a) and stomatopod (Bauer, 1989b) crustaceans
have sophisticated appendages and grooming behaviors designed specifically for removing such epibionts.
Bauer (1989a) provided an excellent review of this
topic, noting that grooming behavior and well-developed grooming appendages are essentially limited to
natant decapods, on which macroscopic fouling is rare.
Significant accumulations of epibiotic microbes could
severely hinder swimming by natant decapods. Reptant
decapods, such as lobsters and brachyuran crabs, do not
have specialized grooming appendages and are frequently observed to have macroscopic fouling by filamentous bacteria such as Leucothrix.
Grooming behavior among smaller crustaceans, such
as copepods, has not been reported, and they do not
appear to have the specialized appendages necessary
for this behavior. Although planktonic copepods are
much smaller than natant decapods (and therefore
exposed to a hydrodynamic regime dominated by viscous forces), heavy fouling from filamentous organisms
would also increase drag and potentially be very detrimental. It is interesting to note that filamentous epibiotic bacteria have not been previously reported on
planktonic copepods from freshwater or marine environments (Table 1). We have observed, however, high
abundances of filamentous bacteria on the planktonic
copepod Labidocera sp. (Fig. 3M) but only at the bases
of its feeding appendages and legs, where they presumably would contribute little to the surface drag of the
animal. Conversely, epibiotic filamentous bacteria are
relatively common among benthic copepods living in
siliceous sand (Fig. 6A), carbonate sand (Figs. 3E, 6B),
or mud (Fig. 6C,D). Indeed, one of us has observed 389
out of 777 (50%) adult female Coullana sp. fouled with
epibiotic filamentous bacteria detectable under low
magnification (3100, light microscopy) (Carman, unpublished) (see Fig. 6C). Conversely, filamentous bacteria
were never detected with light microscopy on a cooccurring species, Pseudostenhelia wellsi. P. wellsi was,
however, found to be commonly colonized with nonfilamentous bacteria (Fig. 3A). We hypothesize that, like
decapods, filamentous bacteria are less detrimental to
benthic copepods than to planktonic forms.
The above argument notwithstanding, the influence
of epibiotic bacteria on copepods is not well understood.
Holland and Hergenrader (1981) suggested that a
mutualistic relationship occurred between freshwater
calanoid copepods and their bacterial epibionts. They
proposed that copepod exoskeletons provide a nutrientrich substrate upon which epibiotic bacteria can flourish; copepods, in turn, may benefit from bacterial
degradation of organic material that might otherwise
131
accumulate on copepod surfaces. Nagasawa (1987) observed pits and scars on copepod exoskeletons that
were clearly the result of activity by chitinoclastic
epibiotic bacteria and thus proposed that epibiotic
bacteria were parasitic on marine calanoid copepods
(Acartia spp.). We have also observed evidence of
chitinoclastic epibiotic bacteria on the planktonic copepod Labidocera sp. (Fig. 4). Other negative effects,
such as interference with mobility or gas exchange
(Bauer, 1989b) could also accrue from epibiotic bacteria.
Hypotheses of mutualistic or parasitic relationships
between copepods and epibiotic bacteria have not been
explicitly tested. There are no data from the literature
to assess Holland and Hergenrader’s (1981) hypothesis
of mutualism. With regards to parasitism, bacterial
degradation of copepod exoskeleton would clearly be
detrimental to the host (Nagasawa, 1987), but chitinoclastic activity by epibiotic bacteria on copepods appears
to be the exception rather than the rule. For example, in
only one of Nagasawa’s several papers concerning
epibiotic bacteria on copepods (Nagasawa, 1987) did
she note the presence of exoskeletal scars from chitinoclastic bacteria. We have examined hundreds of benthic
and planktonic copepods, as well as various other
crustacean taxa, and have found evidence of bacterial
degradation of the exoskeleton only once (Fig. 4). Thus,
we hypothesize that epibiotic bacteria are not, as a rule,
chitinoclastic. If most epibiotic bacteria benefit from the
exploitation of nutrients liberated by living copepods
(see Metabolic Relationships above), it would be adaptive for bacteria not to diminish the longevity of their
host by degrading their exoskeleton. This consideration
would be especially important for the copepod-epibiont
relationship since copepods have a terminal molt and
cannot continuously replace a damaged exoskeleton.
SUGGESTIONS FOR FUTURE RESEARCH
The study of epibiont-host relationships in aquatic
environments is still in its infancy. The population,
community, and biogeochemical implications of epibionthost interactions remain almost entirely unresolved in
marine environments and only slightly less so in freshwater regimes. When these relationships are studied,
several fundamental points of biology must be first
understood, including the epibionts’ species composition, abundance, life histories, attachment mechanisms, and morphologies.
There is a spectrum of functionality among the
microbial epibionts of marine crustaceans. Some protozoans and diatoms (and bacteria?) use the carapace
only as a substrate, without evidence of negative or
positive interaction; we consider such a relationship to
be commensalism. On the other hand, however, some
decapod larvae rely on specific bacteria to prevent
fouling by pathogenic fungi (Gil-Turnes and Fenical,
1992; Gil-Turnes et al., 1989). How do decapods attract
and maintain the helpful bacteria? They must somehow
provide conditions that facilitate the growth of antifungal bacteria while largely excluding others. In these
cases there may be a mutualistic relationship between
the decapods and bacteria; the benefit accrued to the
bacteria, however, has not been demonstrated.
The nature of other functional relationships is less
clear. As noted previously, we see little evidence that
epibiotic bacteria visibly degrade copepod exoskeletons.
Nevertheless, it seems quite possible that epibionts in
132
K.R. CARMAN AND F.C. DOBBS
Fig. 6. Epibiotic filamentous bacteria on benthic (harpacticoid)
copepods. A: Filamentous bacteria on the caudal region of Heteropsyllus nunni. Bar 5 10 µm. B: Filament of cocci attached to Robertsonia
sp. Bar 5 1 µm. C: Low magnification view of Coullana sp. dorsal
urosome. Thread-like structures are long bacterial filaments. Bar 5
100 µm. D: Higher magnification of bacterial filaments in C. Bar 5
20 µm.
general may have some negative effects on their hosts,
as has been demonstrated for some freshwater taxa
(e.g., Threlkeld et al., 1993). At what point do commensal relationships become parasitic, or at least detrimental (e.g., amensalistic)? Perhaps it is a matter of degree,
in which relatively few epibionts do not significantly
influence the substrate organism, but larger epibiont
loads are deleterious. In such cases, how do organisms
unable to groom themselves and having a terminal molt
(e.g., copepods) limit their abundance of epibiotic associates?
Willey and Threlkeld (1995) reported that protozoan
epibiont load is correlated with intermolt duration in
freshwater cladocerans, with longer intermolt periods
resulting in greater accumulations of epibionts. This
phenomenon has not been examined in the marine
environment. The relationship between the abundance
of bacterial epibionts and crustacean intermolt periods
has not been examined in any aquatic environment.
The possibility of coevolved, species-specific relationships between epibionts and hosts should be considered
(e.g., Fenchel, 1965; Chiavelli et al., 1993). Perhaps the
best examples are the apostome protozoans, whose life
cycles are very closely associated with those of their
hosts. This symbiosis is widespread and easily manipulated in the laboratory (e.g., Grimes and Bradbury,
1992), making it a good model for testing hypotheses.
With regard to bacteria, the available evidence suggests that while obligate epibiont-host relationships
may be rare, the epibiont bacterial community may
nevertheless be distinct from free-living bacteria.
Researchers also should be sensitive to spatial and
temporal variability in epibiont-host relationships, as
variability in host availability may strongly influence
population dynamics of epibionts. Again, seasonality
and the epibiont dynamics of an entire community have
been considered in freshwater systems (Chiavelli et al.,
1993) but are virtually unstudied in the marine environment. As a starting point, for example, various pathogenic Vibrio bacteria are known to be highly seasonal in
occurrence and to prefer an epibiotic existence on
crustaceans. Does the crustacean-bacterial symbiosis
function as a vector for potential infection? Are seasonal
fluctuations in Vibrio as well as other bacterial and
nonbacterial epibionts associated with fluctuations in
the availability of zooplankton in general? Are some
MICROBIAL EPIBIONTS ON MARINE CRUSTACEANS
zooplankton species a ‘‘preferred’’ substrate over others? Do epibionts switch between planktonic and benthic hosts? Molecular techniques (e.g., DeLong et al.,
1993) could provide a useful way of determining the
unique character and seasonal variability of epibiotic
bacterial communities associated with crustaceans.
Scientists working in freshwater systems have made
significant progress toward understanding the ecological implications of algal and protozoan epibionts as
they relate to interactions of the host with its predators.
These population- and community-level questions remain largely unexamined in marine systems. In addition to a focus on predation, other approaches, such as
physiological studies of hosts and epibionts, will provide information applicable to higher levels of organization. Collectively, knowledge of positive effects and
negative consequences—to both epibionts and hosts—
may be used to construct predictive, cost-benefit models
for populations and communities.
Finally, the biogeochemical implications of epibiont
associations with copepods and other crustaceans deserve further study. Do epibionts consume disproportionately large amounts of nutrients (organic and inorganic) as they are liberated by their host through
various processes? Are there certain environmental
conditions that favor existence as an epibiont vs. a
free-living microorganism? Do epibionts exhibit physiological traits that allow them to more effectively
exploit nutrients made available by the substrate organism (i.e., are they copiotrophs)?
Our suggestions for future research on microbial
epibionts are by no means exhaustive. We are, however,
convinced that epibionts directly or indirectly have a
significant influence on aquatic communities, and their
study should provide the basis of fruitful and stimulating research.
NOTE ADDED IN PROOF
Since this manuscript’s acceptance in June 1995, the
following articles that are relevant to the topics discussed in this paper have been published.
Additional References:
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ACKNOWLEDGMENTS
We are grateful to the following for their contributions to the images in this manuscript: Donald McGee
and James Cowen (University of Hawaii’s Analytical
EM Facility), Tina Carvalho and Marilyn Dunlap (University of Hawaii’s Biological EM Facility), Ron
Bouchard and Sharon Matthews (Louisiana State University’s Life Sciences EM Facility), Sandy Silver and
Kim Riddle (Florida State University’s EM Facility),
Elizabeth Caetta, and Darcy Lonsdale. We appreciate
critical comments on an earlier draft of this manuscript
by Lisa Drake, Evelyn Gaiser, Barbara Grimes, Darcy
Lonsdale, Michael Montgomery, Stephen Threlkeld,
and Ruth Willey. This work was supported in part by
National Science Foundation grants OCE-90-18599
(Dobbs) and OCE-90-12540 (Lonsdale and Dobbs), a
research and training revolving fund award from the
University of Hawaii (Dobbs), and a grant from the
Louisiana Education Quality Support Fund 1993-95RD-A-03 (Carman).
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