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Sea Turtle Epibiosis

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15 Sea Turtle Epibiosis
Michael G. Frick and Joseph B. Pfaller
15.1 INTRODUCTION
In the marine environment, any exposed, undefended surface will eventually be colonized by marine
propagules (Wahl, 1989). Colonization of inanimate structures (e.g., dock pilings and boat hulls) is
called fouling, while colonization of other marine organisms is called epibiosis. Epibiosis results in
spatially close associations between two or more living organisms (Harder, 2009), in which a single
host (or basibiont) supports one or more typically opportunistic colonizers (or epibionts) (Wahl
and Mark, 1999). Epibiosis is the most common form of symbiosis in the marine environment and
CONTENTS
15.1 Introduction ..........................................................................................................................399
15.2 Common Forms ....................................................................................................................401
15.2.1 Sessile Forms ............................................................................................................401
15.2.2 Sedentary Forms ....................................................................................................... 401
15.2.3 Motile Forms ............................................................................................................401
15.3 Communities and Community Dynamics ............................................................................ 402
15.3.1 Pelagic/Oceanic Communities ..................................................................................402
15.3.2 Benthic/Neritic Communities ...................................................................................402
15.3.3 Obligate Communities ..............................................................................................403
15.3.4 Community Distribution ...........................................................................................403
15.3.5 Community Succession ............................................................................................404
15.4 Ecological Interactions .........................................................................................................405
15.4.1 Effects on Epibionts ..................................................................................................405
15.4.2 Effects on Host Turtles .............................................................................................405
15.4.3 Ecological Inferences ...............................................................................................406
15.4.4 Ecological Implications ............................................................................................407
15.5 Conceptual Model of Epibiosis .............................................................................................408
15.5.1 Geographic Overlap ..................................................................................................408
15.5.2 Ecological Overlap ...................................................................................................408
15.5.3 Balance of Costs and Benets ..................................................................................409
15.6 Considerations ...................................................................................................................... 410
Acknowledgments .......................................................................................................................... 410
15.A Appendix A: Annotated Bibliography of Selected Sea Turtle Epibiont Studies
and Reports Listed by Geographic Region ........................................................................... 411
15.A.1 Caribbean–Western Atlantic..................................................................................... 411
15.A.2 Mediterranean–Eastern Atlantic .............................................................................. 411
15.A.3 IndoWest Pacic ..................................................................................................... 411
15.A.4 Eastern Pacic .......................................................................................................... 412
References ...................................................................................................................................... 412
Bibliography ..................................................................................................................................422
400 The Biology of Sea Turtles, Volume III
may be classied into several types of associations (e.g., mutualism, commensalism, parasitism)
depending on the interactions between a host and its epibionts (Leung and Poulin, 2008).
Sea turtles often act as hosts to a wide variety of epibionts, most of which are unspecialized
organisms normally found associated with inanimate structures in the surrounding marine
environment (i.e., “free living”). These types of epibiotic associations are known as facultative
commensalisms (Wahl and Mark, 1999). That is, the host receives no direct benet from the epibiont
and the epibiont demonstrates little to no substrate specicity. For these associations to occur, the
various settlement cues that facultative commensal epibionts utilize when selecting substrata must
also be present on sea turtles (Zardus and Hadeld, 2004). Alternatively, there are several epibionts
that are found almost exclusively on sea turtles (Frick et al., 2011a). These associations are known
as obligate commensalisms, whereby the epibiont is dependent on the host turtle for survival, but the
welfare of the host turtle is not dependent on the presence or behavior of the epibiont. While some
obligate commensal epibionts are known to perform activities that might be considered benecial
to the host turtle, there are no examples of obligate mutualisms, in which both the host turtle and
the epibiont depend on each other for survival. Future studies, however, may identify such obligate
mutualisms. Most obligate (and facultative) commensal epibionts do not derive nutrients from the
tissue of the host turtle and are not parasitic; instead the host turtle simply provides a foraging
platform (Frick et al., 2002a). On the contrary, several sea turtle epibionts are known to derive
nutrients from the tissue of the host turtle and, therefore, represent associations known as parasitism
(Leung and Poulin, 2008). Parasitic epibionts of sea turtles are rare, but these associations may have
important consequences for the health of host turtles (Greenblatt et al., 2004).
Following a rich history of anecdotal reports dating back to Darwin (1851, 1854), the study of
epibiosis in sea turtles has received considerable attention in recent years. The vast majority of studies
describe the diversity of epibiota, and speculate on the possible causes and effects of these associations.
From these descriptive studies, we have learned a great deal with respect to the wonderful diversity of
epibiotic forms found associated with sea turtles (Appendix A). Fewer studies, however, approach sea
turtle epibiosis from the community perspective. These studies not only describe diversity of epibiota
but also consider the structuring of epibiotic communities and the complex suite of interactions
occurring on the turtle across space and time. Finally, even fewer studies attempt to quantify and
understand the ecological interactions between turtles and their epibiota. These studies have allowed
researchers to better understand the ecological and evolutionary implications of epibiosis, and to
decipher the valuable information that can be gleaned from studying sea turtle epibionts.
Despite the antiquity of some sea turtle epibiont observations, the study of sea turtle epibiosis remains
in a prolonged state of infancy when compared to the breadth of information that has recently and
quickly accrued on sea turtle migrations and home ranges (largely through the deployment of satellite
tags). Likewise, our understanding of sea turtle genetics and molecular phylogeny exceeds that of basic
facets of sea turtle ecology—including diet, foraging behavior, and epibiotic associations. Given the
documented declines of turtle populations in some areas, it has become imperative for scientists to
understand how sea turtles interact with the constituents of the habitats they occupy, be it while foraging
or through epibiosis. Such information allows scientists to view sea turtles within the context of a
complex and ecologically rich marine environment, and it aids in modeling the potential impacts that
certain natural and anthropogenic-driven events may have upon sea turtles and the habitats they utilize.
In this chapter, we begin by introducing many of the common forms of epibionts known to be
associated with sea turtles. Second, we describe several common epibiotic community types, and
discuss the spatial and temporal factors by which epibiotic communities are structured. Third, we
propose a number of costs and benets that may affect sea turtle–epibiont interactions and discuss
the ecological inferences and implications of sea turtle epibiosis. Lastly, we outline a conceptual
model of epibiosis with which researchers may apply to better understand the factors that affect
their particular epibiotic systems and more easily decipher the important biological information that
can be gleaned from studying epibiotic interactions.
401Sea Turtle Epibiosis
15. 2 COMMON FORMS
The diversity of epibionts known from sea turtles is exceptional. For example, loggerhead (Caretta
caretta) and hawksbill turtles (Eretmochelys imbricata) are known to host 200+ and 150+ epibiont
taxa, respectively. For this reason, we have not included an itemized list of epibionts from each
turtle species. Instead, we have included a list of references that include records of epibionts from
sea turtles separated by geographic region (Appendix A) and encourage investigators to examine
the studies cited in this chapter.
15. 2.1 SESSILE FORMS
Sessile forms attach directly to a substrate and do not move around freely. These forms are the most
common and conspicuous epibionts of sea turtles. Most sessile forms have motile, planktonic larvae
that recruit to suitable substrata, where they attach and transform into adults. For these organisms,
the carapace and skin of sea turtles must possess certain settlement cues that larvae recognize,
including water ow characteristics, chemical signals, and surface rugosity. Of the sessile forms
documented from sea turtles, the most noticeable are barnacles (Cirripedia). Barnacles attached
to the carapace of sea turtles are considered “pioneer” species that facilitate the colonization of
subsequent epibiota (see Section 15.3.5; Frick et al., 2002b). Some coronuloid barnacles embed
themselves in the skin and soft tissues of sea turtles (e.g., Chelolepas cheloniae). Through chemical
mediation, these barnacles become encased in connective tissue, which aids in strengthening the
shell of the barnacle while protecting the host tissue from further injury (Frick et al., 2011a). Other
sessile forms include algae, foraminiferans, poriferans, cnidarians (Hydrozoa and Anthozoa),
mollusks (Bivalvia), bryozoans, and tunicates. Many of these sessile forms are colonial and can
reproduce asexually. As a result, some colonies are known to grow quite large and overtake much
of the carapace of the host turtle. In such situations, aggregations of sessile forms provide additional
surface area for the recruitment of other sessile epibiota, and create numerous crevices and spaces
for the colonization of various motile epibionts (see later).
15. 2.2 SEDENTARY FORMS
Sedentary forms live a semi-sessile existence, in which motile individuals construct refugia or
tubes attached to a substrate. Sea turtles host a variety of sedentary forms, including polychaete
worms, amphipods, and tanaids (Frick et al., 1998, 2004b). Some sedentary forms create only
small (1–2 mm long) tubes to dwell in, while others, particularly sabellariid worms and Corophium
amphipods, will aggregate into dense communities—creating reef-like structures consisting of
hundreds of individual tubes bonded together. These “worm reefs” can become quite large (up to
10 cm high) and cover the entire carapace of the host turtle (Frick et al., 2004b). These complex
structures also provide suitable habitat for the colonization of small motile epibionts.
15. 2.3 MOTILE FORMS
Motile forms do not directly attach to a substrate and are capable of free movement throughout
their lives. These organisms may colonize sea turtles directly from the plankton (similar to sessile
forms) or secondarily colonize turtles after initially recruiting to their primary habitat. In the latter
case, colonization may occur when resting turtles contact pelagic or benthic substrata. Motile
forms reported as sea turtle epibionts include protozoans, sipunculid worms, platyhelminth worms,
annelid worms (hirudineans and polychaetes), mollusks (Polyplacophora and Gastropoda), dipterans
(ightless marine midges), decapods (Brachyura, Anomura, Caridea), copepods, ostracods,
peracarids (amphipods, isopods, and tanaids), echinoderms (Ophiuroidea and Echinoidea), and sh
402 The Biology of Sea Turtles, Volume III
(Genera Echeneis and Remora; “shark suckers”). Most motile forms are small and cryptic, and live
within the gaps and sinuses provided by aggregations of sessile and sedentary epibionts. Moreover,
the deposition of sediment between sessile aggregations provides habitat for small infaunal animals
that live in the trapped mud layer (e.g., polychaete worms, amphipods, and clams). For these reasons,
the presence of most motile forms is often dependent on the preceding colonization of other sessile
and sedentary epibiota. Two exceptions are Caprella amphipods, which cling tightly to the host
carapace via limbs with hooked dactyls, and Planes crabs, which hide in the inguinal notch between
the carapace and tail (Chace, 1951). Not surprisingly, these are two of the more common motile
epibionts of sea turtles around the world.
15. 3 COMMUNITIES AND COMMUNITY DYNAMICS
15. 3.1 PEL AGIC/OCEANIC COMMUNITIES
All extant sea turtles, except the atback turtle (Natator depressus), utilize pelagic and oceanic
habitats during juvenile life stages (Bolten, 2003) and some continue to use these habitats throughout
adulthood (e.g., Dermochelys coriacea and eastern Pacic Lepidochelys olivacea). Adult and
subadult loggerhead turtles (C. caretta) are considered mostly neritic, but some individuals make
occasional forays into the pelagic/oceanic environment (Frick et al., 2009; Reich et al., 2010). During
pelagic/oceanic life stages, sea turtles may host communities of pelagic organisms that are typically
found associated with drifting otsam (e.g., Sargassum) and jetsam. These organisms primarily
include pedunculate barnacles of the genera Lepas and Conchoderma, and grapsid crabs of the
genus Planes. Lepas spp. and Conchoderma spp. are ubiquitous throughout the world’s oceanic
environment and are known to colonize a variety of other nektonic hosts (e.g., Reisinger and Bester,
2010; Pfaller et al., 2012). Studies on Planes crabs from oceanic-stage sea turtles represent the most
detailed information on sea turtle–epibiont symbiosis to date (Davenport, 1994; Dellinger et al.,
1997; Frick et al., 2000a, 2003b, 2004a, 2006, 2011b; Pons et al., 2011). Other less frequent epibionts
of the pelagic/oceanic community may include pelagic sea slugs (Fiona pinnata), sea spiders
(Endeis spinosa), pelagic tunicates (Diplosoma gelatinosum), and crabs of the genera Portunus
and Plagusia (Frick et al., 2003a, 2011b; Loza and López-Juardo, 2004). The presence of pelagic/
oceanic epibionts on sea turtles outside these areas strongly suggests that these turtles have recently
migrated from the pelagic/oceanic environment, providing valuable insights into cryptic migratory
behaviors and habitat preferences of sea turtles.
15. 3. 2 BENTHIC/NERITIC COMMUNITIES
After early life stages in pelagic/oceanic areas, most cheloniid sea turtles transition to more
coastal and benthic habitats—presumably in search of food, and later for mates (Bjorndal, 1997).
In benthic/neritic habitats, sea turtles become exposed to intense colonization pressure by marine
propagules (larvae and spores) seeking to colonize submerged substrata and begin their benthic
existence. The skin and especially the carapace of sea turtles provide suitable substrata for a variety
of benthic/neritic organisms (Frick et al., 1998, 2000a; Schärer, 2001). As previously mentioned,
the recruitment of sessile and sedentary forms (e.g., barnacles, tubicolous worms, and tunicates)
facilitates the colonization of smaller motile forms (e.g., crabs, amphipods, mollusks, etc.), which
inhabit the gaps and crevices between sessile aggregations. After prolonged exposure to settlement
by local plants and animals in a given area, the epibiotic communities of sea turtles begin to
resemble the adjacent benthic environment. For this reason, the species composition of benthic/
neritic communities is largely dependent on the geographic region or habitat in which the host turtle
occupies (Frick et al., 1998; Schärer, 2001). Complex benthic/neritic communities are most evident
on nesting female turtles, which tend to remain relatively sedentary and localized during the nesting
period (Frick et al., 2000b).
403Sea Turtle Epibiosis
15. 3. 3 OBLIGATE COMMUNITIES
Obligate communities are composed almost entirely of organisms that are known exclusively as
epibionts of sea turtles and other motile marine organisms. That is, these communities are largely
independent of the habitat in which the turtle occupies (i.e., pelagic/oceanic vs. benthic/neritic). The
predominant epibiont of obligate communities is the coronuloid barnacle Chelonibia testudinaria.
This ubiquitous species is the most frequently reported epibiont of sea turtles and is also known
to colonize crabs, sirenians, and crocodilians (Newman and Ross, 1976; Zardus and Hadeld,
2004; Cupul-Magaña et al., 2011; Nifong and Frick, 2011). Chelonibia testudinaria occurs in
great numbers on some turtles and appears to function as a “pioneer” for the development of more
extensive and diverse epibiotic communities (Frick et al., 2002b; Rawson et al., 2003). Aggregations
of C. testudinaria provide refugia for other obligate epibionts, such as the ruby-eyed amphipod
(Podocerus chelonophilus) and the robust tanaid (Hexapleomera robusta). However, both species
will also cling directly to the skin and carapace of host turtles, and P. chelonophilus will also
aggregate around epidermal lesions and eat necrotic tissue from the wounds of host turtles (Moore,
1995). Other obligate epibionts of sea turtles include marine red alga (Polysiphonia carettia), which
is known only from cheloniid sea turtles (Senties et al., 1999), and several other species of coronuloid
barnacles that are wholly chelonophilic (Ross and Frick, 2011). While some individual turtles are
known to host strictly obligate communities (Frick et al., 2010a), most communities composed
primarily of obligate epibionts also contain some facultative forms.
15. 3. 4 COMMUNITY DISTRIBUTION
The spatial distribution of epibiont communities on host turtles may be inuenced by a complex
suite of factors, including recruitment dynamics, water ow patterns, differential disturbance among
body regions, and inter- and intraspecic interactions (Pfaller et al., 2006). In general, studies that
examine or anecdotally report on the distribution of sea turtle epibionts have found that epibiont
communities tend to aggregate on the carapace, as opposed to the skin or plastron (Gramentz,
1988; Fuller et al., 2010). Extra-carapacial epibionts mostly include barnacles, parasitic leeches,
and Planes crabs (Chace, 1951; Gramentz, 1988; Frick et al., 1998; Hayashi and Tsuji, 2008). Some
barnacles occur only along the plastral sutures (e.g., Stomatolepas transversa) (Young, 1991), while
others mostly occur along the leading edges of the front ippers (e.g., Stephanolepas muricata)
(Frick et al., 2011a). Limb movements, unfavorable water ow patterns, and the sloughing of skin
by the host turtle probably restrict the recruitment and development of extra-carapacial epibionts.
Nevertheless, information on the distributions of extra-carapacial epibionts is still lacking (Frick
et al., 2011a).
Most studies that examine the spatial distribution of epibiont communities on sea turtles have
focused on the carapace, where the densest and most diverse communities are found (Frick et al.,
1998). These studies indicate that epibiotic communities tend to be distributed in nonrandom patterns.
Most studies report a tendency for epibiont communities to cluster along the vertebral scutes and
across the posterior third of the carapace (Caine, 1986; Matsuura and Nakamura, 1993; Frick et al.,
1998; Pfaller et al., 2006). Such nonrandom distributions are thought to reect the preference of
lter-feeding epibionts (e.g., barnacles) for elevated ow rates along the vertebral scutes and the
favorable settlement conditions for other epibiota along the posterior of the carapace where ow rates
are reduced (Pfaller et al., 2006). Recruitment of “pioneer” species in these areas (e.g., Chelonibia
barnacles and Polysiphonia alga) will then facilitate the accumulation of more diverse epibiotic
communities (Gramentz, 1988; Frick et al., 2000b; Fuller et al., 2010). Additionally, the colonization
and persistence of epibionts on the anterior costal scutes may be reduced by contact from the front
ippers (Caine, 1986; Dodd, 1988) and/or removal during “self-grooming” (Schoeld et al., 2006;
Frick and McFall, 2007). Other studies show mostly random distributions among barnacle species
with some spatial structuring among different size classes of barnacles (Fuller et al., 2010).
404 The Biology of Sea Turtles, Volume III
Recently, Moriarty et al. (2008) conrmed that the obligate commensal barnacle, Chelonibia
testudinaria, is capable of substantial (but slow) post-settlement locomotion. Individual C.
testudinaria were shown to move across multiple scutes from areas of low water ow to areas with
better lter-feeding conditions. Such movements may be triggered by differential ow rates over the
carapace or/and the presence of conspecics that disrupt ow patterns. As previously mentioned,
Chelonibia spp. are important “pioneer” species for epibiotic communities (Frick et al., 2000) and
post-settlement locomotion will certainly affect the spatial distribution of epibiotic communities.
However, as the density of C. testudinaria and other epibiota increases, post-settlement locomotion
and survival will be reduced, and the overall distribution may become more reective of differences
in recruitment patterns (Pfaller et al., 2006).
Debilitated turtles will host epibionts, especially barnacles, over their entire external surface
area—including portions of the mouth regularly exposed to the outside environment. These
“barnacle bill” turtles will often suffer severe deformations as a result of barnacle colonization.
Current information indicates that such turtles are immunosuppressed or lethargic prior to barnacle
colonization and that limited mobility by the host likely facilitates rapid and prolic colonization
of barnacles (Deem et al., 2009). Nevertheless, because healthy turtles may also support massive
aggregations of epibionts over much of their bodies, it is difcult to judge the health of a turtle
simply by examining epibiont loads and percentage coverage (see Deem et al., 2009).
15. 3. 5 COMMUNITY SUCCESSION
Prior to the colonization of macroorganisms, all structures exposed to seawater initially undergo
a similar sequence of events (Wahl, 1989): (1) biochemical conditioning, whereby surfaces absorb
dissolved macromolecules; (2) bacterial colonization; and (3) unicellular eukaryote (e.g., yeasts,
protozoa, and diatoms) colonization. To our knowledge, these critical stages in the process of
epibiosis in sea turtles have never been explored.
The temporal succession of “macro”-epibiont communities on host turtles remains poorly
understood, as well. To date, there is one study that examines temporal succession of epibiont
communities from individual turtles over an extended period of time (Frick et al., 2002b). Using,
ipper-tagging data, photography, and in situ assessments, epibiont data were collected from the
carapaces of nesting loggerhead turtles (C. caretta) in Georgia, United States, over the course
of 3 months. General observations of community succession were similar to those reported for
neritic, epibenthic communities (Dean, 1981). Community succession is typically initiated when
hard, sessile forms like barnacles (C. testudinaria in Frick et al., 2002b) colonize a relatively
bare carapace. These “pioneers” facilitate the subsequent colonization of other epibiota by
increasing the surface area for colonization and changing water ow patterns (Pfaller et al.,
2006). Secondary colonizers include other sessile forms (e.g., hydrozoans and bryozoans) and
sedentary forms, which take refuge within the interstices of the barnacles (e.g., tanaids). The
accumulation of sediments among primary and secondary sessile forms then facilitates the
colonization of sessile tunicates and many small, motile forms. Tunicates and other secondary
sessile forms tend to overgrow and kill the barnacles beneath them. Tunicates (Molgula
manhattensis) appear to be the climax species of the carapace epibiont community on nesting
loggerheads in Georgia, United States. Aggregations of M. manhattensis occasionally cover the
entire carapace at the end of the season, providing innumerable gaps and crevices for a diverse
array of motile epibionts.
At or before reaching terminal succession, epibiont communities may be partially or
catastrophically disturbed by various biotic and abiotic factors. Turtles that accumulate benthic/
neritic communities may immigrate to different, less favorable habitats, causing the less tolerant
epibionts to die and slough off. In some cases, this may completely clear the carapace of epibiota.
Moreover, community succession may be disrupted when host turtles “groom” themselves
by actively rubbing against submerged structures to remove epibiota (Heithaus et al., 2002;
405Sea Turtle Epibiosis
Schoeld et al., 2006; Frick and McFall, 2007). Evidence of such behaviors is often present in the
form of longitudinal scratch marks on the carapace (Caine, 1986; Frick and McFall, 2007). Lastly,
predatory epibionts (e.g., Planes crabs and several gastropods) and sh may systematically clean/
remove certain epibionts (Davenport, 1994; Losey et al., 1994; Frick et al., 2000a, 2011b; Pfaller
et al., 2008; Sazima et al., 2010). These factors may lead to partial or complete turnover of the
epibiotic communities of sea turtles.
15. 4 ECOLOGICAL INTERACTIONS
15. 4.1 EFFECTS ON EPIBIONTS
Epibionts may benet from epibiosis through reduced competition and predation. These are major
factors affecting the ability of marine propagules to successfully colonize a substratum (Enderlein
and Wahl, 2004). Thus, when risk of predation is high or when settlement area is limited—whether
by high population densities (e.g., on benthic structures) or by low substrata availability (e.g., on
pelagic otsam)—epibiosis of sea turtles may be benecial for the survival of marine propagules
(Wahl, 1989; Pfaller et al., 2012). Some “burrowing” barnacles may avoid predation by encasing
themselves within the tissue of host turtles via chemical mediation (Frick et al., 2011b). Epibionts
may also benet from improved energetic positioning. Filter-feeding epibionts, such as barnacles,
may benet from favorable feeding currents on host turtles (Pfaller et al., 2006), while photosynthetic
epibionts, such as algae, may benet from increased oxygen and light availability (Shine et al.,
2010). Furthermore, epibionts may benet though range expansion and increased genetic mixing by
hitchhiking on migratory turtles (termed phoresis). Researchers have hypothesized that sea turtles
may act as long-distance dispersal vectors for benthic marine invertebrates (Schärer and Epler,
2007; Harding et al., 2011).
Epibiosis may be costly to epibionts when turtle behaviors cause physical disturbance and
unfavorable uctuations in physiological conditions (Wahl, 1989). Contact between turtles during
mating, or between turtles and submerged structures (e.g., rock or coral ledges), may physically
damage epibionts, especially those with fragile, erect body forms (e.g., leafy bryozoans and soft
corals). As previously mentioned, sea turtles are also known to actively remove epibionts by scraping
against submerged structures (Heithaus et al., 2002; Schoeld et al., 2006; Frick and McFall, 2007).
Moreover, epibionts that are sensitive to desiccation may die when turtles emerge to nest or bask at
the surface (Caine, 1986; Bjorndal, 2003). Similarly, epibionts that are sensitive to uctuations in
temperature, salinity, or pressure may not survive when turtles migrate and/or dive. Another cost
for certain epibionts might be reduced access to food resources and mates, which would ultimately
cause reduced longevity and reproductive capacity. These costs might favor epibionts capable of
asexual reproduction and dietary versatility.
15. 4. 2 EFFECTS ON HOST TURTLES
Epibiosis may be costly to host turtles when epibionts cause increased weight and drag. In
extreme cases, epibiotic loads have been reported that effectively double the mass and volume of
juvenile sea turtles (Bolten unpubl. data in Bjorndal, 2003). Epibionts attached to the carapace
may increase drag by disrupting the laminar ow over the carapace (Logan and Morreale, 1994)
and those embedded in the leading edge of the front ippers may increase drag while swimming
(Wyneken, 1997; Frick et al., 2011a). The energetic costs of hosting epibionts are likely greatest
when turtles undertake long-distance migrations and least when turtles remain relatively sedentary
(e.g., females during internesting periods). Because otherwise healthy turtles will often support
massive epibiont aggregations (Deem et al., 2009), turtles are apparently capable of overcoming
the costs associated with “epibiotic drag” and should not be judged as healthy or unhealthy
simply by examining epibiotic loads (see Deem et al., 2009). Furthermore, the aforementioned
406 The Biology of Sea Turtles, Volume III
“barnacle bill” turtles tend to accumulate their prolic barnacle loads after (not before) becoming
lethargic at the surface.
Epibiosis may also be costly to host turtles when certain epibionts detrimentally affect the health
of host turtles. A number of common epibionts of sea turtles (e.g., platyhelminth worms, annelid
worms and barnacles) are thought to be the cause of or related to infections of sea turtles (George,
1997; Alfaro, 2008). Tissue damage caused by burrowing epibionts may increase the vulnerability
of host turtles to pathogens (George, 1997). Some coronuloid barnacles (e.g., C. cheloniae, S.
muricata, and Cylindrolepas darwiniana) become embedded within hard and soft tissues of host
turtles causing deep-tissue wounds that can sometimes leave impressions on the underlying bone
(Hendrickson, 1958; Green, 1998; Frick and Zardus, 2010; Frick et al., 2010a). Platylepas decorata
have also been found imbedded in the beaks of host turtles causing severe beak deformation, which
may lead to reduced foraging capacity and death of the host turtle (see Green, 1998; Frick and
Zardus, 2010). Other non-barnacle forms may act as disease vectors of pathogens. Parasitic marine
turtle leeches (Ozobranchus sp.) not only consume host tissue but also are believed to act as disease
vectors for the dispersal of the bropapilloma-associated herpes virus found in latent tumors that
often cover, deform, and debilitate host turtles (Greenblatt et al., 2004). Commensal gastropods of
sea turtles may act as intermediate hosts for spirorchiid blood ukes (Frazier et al., 1985), which can
have devastating effects on host turtles (George, 1997).
Host turtles may benet from epibiosis through improved optical, chemical, or electrical
camouage. Predators may not recognize hosts as potential prey items if epibiotic communities
visually or chemically resemble the surrounding benthic communities (Rathbun, 1925; Fishlyn and
Phillips, 1980; Feifarek, 1987; Frazier et al., 1991). Moreover, dense epibiotic communities may
disrupt electric elds produced by hosts, allowing hosts to avoid predation by predators that utilize
electrolocation when searching for prey (e.g., sharks) (Ruxton, 2009). Hosts may also benet from
epibiosis through associational defense and cleaning. Epibionts with chemical or structural defenses
(e.g., toxins, sharp projections, or hard outer coverings) may deter predation on host turtles (Wahl
and Mark, 1999; Bjorndal, 2003). Predatory epibionts may provide a cleaning benet by consuming
other epibionts—some of which may be harmful—from the surface of host turtles (Davenport,
1994; Sazima et al., 2010).
15. 4. 3 ECOLOGICAL INFERENCES
Studies of epibiosis have helped elucidate cryptic life history attributes of sea turtles and informed
the implementation of conservation measures. While such studies will not and should not supplant
the use of tag-return data, satellite telemetry, stable-isotope analyses, or population genetics,
studying epibiosis can provide a time- and cost-effective alternative to elucidate the geographic
ranges, habitat preferences, and migratory corridors of sea turtles. Using primarily examples from
the well-studied epibiont community of loggerhead turtles in the northwestern Atlantic Ocean,
we illustrate the types of ecological inferences that can be gained by studying the epibionts of
sea turtles.
Epibiont data have been used to elucidate the foraging locations of loggerhead turtles nesting
along the Atlantic coast of Florida, United States. These turtles occasionally host epibionts that are
geographically restricted to far southern Florida, the Bahamas, and the Caribbean (Caine, 1986;
Pfaller et al., 2008). Such associations suggest that these nesting turtles had recently migrated from
more southerly areas where their range overlapped with free-living populations of the epibionts.
Data from ipper-tag returns, satellite telemetry, and stable-isotope analyses have conrmed
that turtles nesting in Florida frequently utilize these more southerly, tropical waters during
nonbreeding seasons (Meylan, 1983; Foley et al., 2008; Pajuelo et al., 2012). Caine (1986) further
extrapolated these epibiont data to suggest the presence of two discrete nesting assemblages along
the southeastern United States, one to the north and one to the south of Daytona Beach, Florida
(approximately 29° N latitude). Several years later this hypothesis was rather precisely conrmed by
407Sea Turtle Epibiosis
molecular data (Bowen et al., 1993; Encalada et al., 1998) and now these two nesting assemblages
receive markedly different conservation status (Turtle Expert Working Group, 2009).
In another example from nesting loggerhead turtles in Florida, United States, Reich et al. (2010)
supplemented stable-isotope data with epibiont community data to suggest a bimodal foraging
strategy by female loggerheads prior to their arrival at breeding grounds. Because isotopic signatures
(depleted vs. enriched δ13C) can vary along multiple environmental continua, the incorporation of
epibiont data in this study provided additional support for an oceanic versus neritic dichotomy,
as opposed to dietary or latitudinal gradients. These results have important implications for role
of adult loggerhead turtles in the oceanic environment and the management policies that serve to
protect them.
Epibiont data have also been used to assess the foraging migrations of juvenile and subadult
loggerhead turtles. Killingley and Lutcavage (1983) used duel isotopic proles (δ18O and δ13C) from
the shells of C. testudinaria to reconstruct the movements of subadult loggerheads between oceanic
habitats in the northwest Atlantic and estuarine habitats in the Chesapeake Bay (Maryland and
Virginia). Moreover, Limpus and Limpus (2003) used the presence of particular epibionts (Planes
sp. and S. muricata) and morphological features to identify which juvenile turtles caught in neritic
habitats in the southwest Pacic Ocean had recently recruited from the open ocean. In both studies,
epibiont data provided valuable insights in to cryptic host movements that otherwise would have
been very difcult to obtain.
Lastly, in another interesting application of epibiont data, Eckert and Eckert (1988) measured
the size distribution of epibiotic barnacles (Conchoderma virgatum) on nesting leatherback turtles
to extrapolate the time of arrival to the tropical nesting region. Because reproduction in these
barnacles is typically restricted to tropical regions, their colonization of turtles is limited to the
period when turtles also occupy tropical waters. Based on reproductive periodicity and established
growth rates of barnacles (Eckert and Eckert, 1987), the authors determined that turtles do not
arrive from temperate latitudes until just prior to nesting and orient directly toward their preferred
nesting beach (Eckert and Eckert, 1988). These data have provided important information on the
cryptic migratory behavior of leatherback turtles and have better informed the implementation of
conservation measures.
15. 4. 4 ECO LOGICAL IMPLICATIONS
The ecological implications of sea turtle epibiosis remain one of the most poorly understood aspects
of this nascent eld. Aside from many of the direct effects of epibiosis on host turtles and epibionts
discussed earlier (Sections 15.4.1 and 15.4.2), sea turtle epibiosis may have other less obvious,
indirect effects on the marine communities and habitats that sea turtles inhabit.
Several authors have discussed the potential role of sea turtles as dispersal vectors for a
diverse array of marine invertebrates over broad geographic regions (Bjorndal and Jackson,
2003; Schärer and Epler, 2007; Harding et al., 2011; Lezama et al., 2012). Hitchhiking on highly
mobile hosts may facilitate genetic mixing and/or range expansion for epibionts capable of
reproducing on turtles or after arriving in distant locations (Rawson et al., 2003). These factors
may be particularly important for invertebrate taxa with limited dispersal capacities (Schärer
and Epler, 2007). Turtle-mediated genetic mixing may aid in maintaining the genetic diversity
and homogeneity of marine invertebrate populations (Rawson et al., 2003), but may also inhibit
biological diversication by impeding local adaptation or random divergence. Moreover, turtle-
mediated range expansion may promote biological diversication if newly established populations
subsequently remain isolated from their source populations, or disrupt ecosystem functioning
when invaders compete with or consume resident species.
A recent study has drawn attention to the potential for turtle-mediated introductions of
nonindigenous and potentially invasive species. Harding et al. (2011) report the rst records of the
nonindigenous veined rapa whelk (Rapana venosa) as an epibiont of loggerhead turtles in Virginia
408 The Biology of Sea Turtles, Volume III
and Georgia. R. venosa is a generalist shellsh predator native to Asia that has recently been
introduced in to the Chesapeake Bay (Harding and Mann, 1999). However, the size and stage of the
epibiotic individuals on turtles in Georgia indicate the presence of an extra-Chesapeake breeding
population of this invasive species. The authors suggest that turtle-mediated dispersal is currently
the only compelling explanation for the occurrence of R. venosa on turtles in Georgia. These
ndings have important implications for the future management of invasive marine invertebrates.
Sea turtles are known to modify the physical structure of their habitat in a number of ways
(Bjorndal and Jackson, 2003). Thus, another unexplored ecological implication of sea turtle
epibiosis might be the extent to which turtles modify hard-bottom habitats when actively
removing epibiota. This behavior involves turtles pushing their carapace against the underside of
rock ledges and vigorously scrapping against the rock to remove epibiota, particularly barnacles
(Frick and McFall, 2007). The rock ledges often erode during such behaviors, leaving behind
scours or arched ledges, which turtles may return to for subsequent “self-grooming.” The extent
to which these habitat modications affect the surrounding reef or hard-bottom communities
remains unknown.
15. 5 CONCEPTUAL MODEL OF EPIBIOSIS
As we accumulate studies of epibiotic diversity in sea turtles, we have begun to formulate a
conceptual framework to better understand and learn from these epibiotic interactions. While
there have been several broad reviews on epibiosis (see Wahl, 1989; Wahl and Mark, 1999; Harder,
2009; Wahl, 2009), there has been no attempt to construct a conceptual framework to explain such
associations. The conceptual model of epibiosis depicted in Figure 15.1 outlines three hierarchical
factors inherent to epibiotic interactions: (1) geographic overlap (Figure 15.1A), (2) ecological
overlap (Figure 15.1B), and (3) the balance of costs and benets to hosts and epibionts that dictate
the likelihood of epibiosis once in close proximity (Figure 15.1C). Because the factors that affect
epibiotic interactions—as displayed in this conceptual model—are inherent to the biology of the
species involved, we can learn about the ecology and evolution of these species by studying epibiosis.
Such a conceptual framework will hopefully allow researchers to better understand the factors
that affect their particular epibiotic systems and more easily decipher the important biological
information that can be gleaned from studying epibiosis in sea turtles.
15. 5.1 GEOGRAPHIC OVERLAP
A necessary prerequisite for epibiosis is geographic overlap between the range of the host turtle and
the range of the epibiont (Figure 15.1A). Logically, without geographic overlap, epibiosis between a
host turtle and any potential epibiont would never occur. This is an obvious criterion for epibiosis.
However, because the host turtles are highly mobile, the occurrence of particular epibiont taxa
with more limited distributions can reveal information about cryptic host movements. Studies of
sea turtle epibionts have provided important information on the migratory behavior of loggerhead
and leatherback turtles (Caine, 1986; Eckert and Eckert, 1988), and subsequently informed the
implementation of conservation measures.
15. 5. 2 ECOLOGICAL OVERLAP
Where geographic ranges overlap, epibiosis will then depend on the spatial and temporal overlap
in ecology of the host turtles and potential epibionts (Figure 15.1B). Local geographic areas are
typically heterogeneous mosaics of different habitats, each characterized by different ecological
communities of plants and animals (e.g., saltmarshes, coral reefs, pelagic areas). The species
composition of local communities may also vary through time, especially for seasonal differences
409Sea Turtle Epibiosis
in recruitment of larval propagules. Host turtles may utilize many different habitats or may show
preferences for certain habitats during different behaviors (e.g., foraging, resting, and mating) or
life stages, or at different times of the year. In order for epibiosis to occur, the host turtles must
occupy the same habitat at the same time as free-living populations of potential epibionts. Thus, the
epibionts associated with a given host turtle should reect the assemblage of plants and animals that
occupy the habitats where the hosts spend time. For example, sea turtles that tend to inhabit benthic/
neritic habitats tend to host different epibionts than turtles that tend to inhabit pelagic/oceanic
habitats (Limpus and Limpus, 2003; Reich et al., 2010). Such information can be used to assess
interspecic and intraspecic differences in habitat use, which is critical for the implementation of
effective conservation strategies.
15. 5. 3 BALANCE OF COSTS AND BENEFITS
Once in close proximity, there is a complex balance of costs and benets for host turtles and
potential epibionts that ultimately determine the likelihood of epibiosis. Figure 15.1 displays a
2D likelihood surface in which each axis represents a continuum from high benet to high cost.
The various positions of different hosts and epibionts along these cost-benet axes depend on
the net cost or benet experienced during epibiosis. Because the relative costs and benets are
(A)
Geographic
overlap
Host
Range
Epibiont
Range
(B)
Ecological
overlap
Epibiont
Ecology
Host
Ecology
(C)
Bepibiont
Cepibiont
Low High
Likelihood of epibiosis
Chost B
host
III
III IV
FIGURE 15.1 Conceptual model of epibiosis. (A,B) Venn diagrams showing the geographic and ecological
overlap between hosts and epibionts, respectively. (C) Graph showing the likelihood of epibiosis based on the
balance of cost and benets to hosts and epibionts (Bepibiont, benet to the epibiont; Bhost, benet to the host;
Chost, cost to the host; Cepibiont, cost to the epibiont).
410 The Biology of Sea Turtles, Volume III
different for different turtle–epibiont pairs, some associations are more likely and therefore more
frequent than others. Epibiotic interactions in which both species experience a net benet would
have a high likelihood of occurring and therefore would be more frequent (quadrant I). Such
mutually benecial associations would favor mechanisms for active attraction and may develop
into obligate associations over evolutionary time. On the other end of the continua, interactions
in which both species suffer high costs would have a low likelihood and would effectively never
occur (quadrant III). Interactions in which one species incurs a high cost while the other receives
minimal benet would also have a low likelihood (bottom left of quadrants II and IV), as the
former species would actively avoid such interactions and the latter would gain very little by
exploiting the former. Conversely, if one species receives a high benet at a high cost to the
other species (top left of quadrant II and bottom right of quadrant IV), then such associations
might exhibit patterns similar to that of parasitic interactions (top left of quadrant II only). Lastly,
interactions in which one species receives a high benet while the other incurs little or no cost
would have a higher likelihood and would be relatively frequent (top left of quadrants II and IV).
This last scenario characterizes many of the interactions between sea turtles and their epibiota,
and is typically referred to as commensalism (Leung and Poulin, 2008).
As previously mentioned, epibionts may benet from epibiosis through reduced spatial
competition and predation (Wahl, 1989; Enderlein and Wahl, 2004; Pfaller et al., 2012), improved
energetic positioning (Pfaller et al., 2006; Shine et al., 2010), and range expansion (Schärer and
Epler, 2007; Harding et al., 2011), while coping with costs associated with physical disturbance
(Wahl, 1989; Schoeld et al., 2006; Frick and McFall, 2007), transport to unfavorable physiological
environments (Caine, 1986; Bjorndal, 2003), and reduced access to food resources and mates.
Host turtles may benet from epibionts through optical, chemical, or electrical camouage
(Rathbun, 1925; Fishlyn and Phillips, 1980; Feifarek, 1987; Frazier et al., 1991; Ruxton, 2009)
and associational defense and cleaning (Davenport, 1994; Wahl and Mark, 1999; Bjorndal,
2003), while coping with costs associated with increased weight and drag (Logan and Morreale,
1994; Bjorndal, 2003), and tissue da mage and associated susceptibility to pathogens (George,
1997; Greenblatt et al., 2004). The balance of costs and benets to host turtles and epibionts will
ultimately determine the likelihood—and therefore the frequency—of epibiosis for most turtle–
epibiont associations.
15. 6 CONSIDERATIONS
Studies that seek to elucidate the relationships that exist between sea turtles and other marine
organisms require investigators to adopt an interdisciplinary approach to data collections and
analyses. Knowledge of the standard measurements and preservation methods employed by taxon
specialists is important to properly report and archive marine algae and invertebrate specimens
(Lazo-Wasem et al., 2011). A familiarity with the life histories and general biology of the marine
organisms that utilize the habitats occupied by sea turtles is essential for identifying situations that
bring sea turtles into contact with the marine organisms they consume and those that attach to
them. An understanding of the major systematic characters that dene the major family-groups of
local marine ora and fauna is helpful for identication, and to adequately ascertain evolutionary
relationships between sea turtles and other marine organisms.
ACKNOWLEDGMENTS
We sincerely thank Rebecca Pfaller for valuable editorial and technical assistance. We thank
Kristina L. Williams of the Caretta Research Project, Karen Bjorndal, Alan Bolten, Peter Eliazar,
and our other colleagues at the Archie Carr Center for Sea Turtle Research for their encouragement,
advice, and support, and we greatly appreciate the helpful comments of anonymous reviewers that
improved an earlier draft of the present chapter.
411Sea Turtle Epibiosis
15. A APPENDIX A: ANNOTATED BIBLIOGRAPHY OF SELECTED SEA TURTLE
EPIBIONT STUDIES AND REPORTS LISTED BY GEOGRAPHIC REGION
15. A.1 CARIBBEAN–WESTERN ATLANTIC
Bacon, 1976 (Trinidad); Bugoni et al., 2001 (Rio Grande do Sul: Brazil); Cardenas-Palomo and
Maldonado-Gasca, 2005 (Yucatan: Mexico); Caine, 1986 (South Carolina, Florida); Farrapeira-
Assunção, 1991 (Brazil); Frazier et al., 1985 (Georgia, Florida); Frazier et al., 1991 (Georgia);
Frazier et al., 1992 (Georgia; Rio Grande do Sul: Brazil); Frick et al., 1998 (Georgia); Frick and Slay,
2000 (Georgia); Frick and Zardus, 2010 (Panama, Georgia, and Florida); Frick et al., 2000a, 2000b
(Georgia); Frick et al., 2002a,b (Georgia); Frick et al., 2003a (Jumby Bay: Antigua); Frick et al.,
2004b (Georgia); Frick et al., 2006 (Florida); Frick et al., 2010a (Nova Scotia, Georgia); Frick
et al., 2010b (Georgia and Florida); Gruvel, 1905 (Antilles Sea); Henry, 1954 (Florida, Texas);
Hunt, 1995 (Florida); Ives, 1891 (Yucatan: Mexico); Killingley and Lutcavage, 1983 (Virginia);
Lutcavage and Musick, 1985 (Virginia); Nilsson-Cantell, 1921 (Florida); Nilsson-Cantell, 1939
(Bay of Chacopata: Venezuela); Pereira et al, 2006 (Almofala: Brazil); Pilsbry, 1916 (Cape Frio:
Brazil; Delaware, Florida, New Jersey; Point Patuca: Honduras; West Indies); Plotkin, 1996
(Texas); Richards, 1930 (New Jersey); Rudloe et al., 1991 (Florida); Schwartz, 1960 (Maryland);
Walker, 1978 (North Carolina); Wass, 1963 (Virginia); Wells, 1966 (Florida); Weltner, 1897
(Florida; Cuba; Bahia: Brazil); Young, 1991 (Brazil); Zavodnik, 1997 (Rovinj: Croatia); Zullo and
Bleakney, 1966 (Massachusetts; Nova Scotia: Canada); Zullo and Lang, 1978 (South Carolina).
15. A.2 MEDITERRANEAN EASTERN ATLANTIC
Badillo-Amador, 2007 (Mediterranean Sea); Barnard, 1924 (Table Bay: South Africa); Broch, 1924
(Baie du Levrier: Mauretania; Gambia); Broch, 1927 (Rabat: Morocco); Carriol and Vader, 2002
(Finmark: Norway); Caziot, 1921 (Nice: France); Chevereaux and de Guerne, 1893 (between Algeria
and Balaeres); Darwin, 1854 (Africa; Mediterranean Sea); Davenport, 1994 (Madeira); Frazier et al.,
1985 (Peloponnesus, Zakynthos Island: Greece); Frick et al., 2010a (Gabon: Africa); Gauld, 1957
(Accra: Ghana); Geldiay et al., 1995 (Koycegiz-Dalyankoy: Turkey); Gramentz, 1988 (Malta, Zacharo,
Zakynthos: Greece; Lampedusa: Italy); Gruvel, 1903 (Palermo: Italy; Alexandria: Egypt); Gruvel, 1931
(Gulf of Alexandrette); Haelters and Kerckhof, 1999 (DeHaan: Belgium); Haelters and Kerckhof, 2001
(Oostende: Belgium); Holothuis, 1952 (Ouddorp: the Netherlands); Holothuis, 1969 (Ameland Island: the
Netherlands); Kitsos et al., 2005 (Aegean Sea); Kolosvary, 1939 (Rovigno, d’Istria: Croatia); Kolosvary,
1943 (Alexandria: Egypt; Palermo, Sicily: Italy); Kolosvary, 1951 (Mediterranean Sea); Koukouras
and Matsa, 1998 (Aegean Sea; Levantine Basin); Lanfranco, 1979 (St. Julians: Malta); Lucas, 1968
(Mediterranean Sea); Margaritoulis, 1985 (Zakynthos: Greece); Nilsson-Cantell, 1921 (Bibundi:
Cameroon); Nilsson-Cantell, 1931 (Mediterranean Sea); O’Riordan, 1979 (Dingle: Ireland); O’Riordan
and Holmes, 1978 (Ventry Harbor: Ireland); Pilsbry, 1916 (Taranto: Italy; Cape of Good Hope: South
Africa); Quigley and Flannery, 1993 (Dingle Bay: Ireland); Relini, 1968 (Gulf of Trieste: Italy); Relini,
1969 (Adriatic Se a); Relini, 1980 (Adriat ic Sea); Sezgin et al., 2009 (Turkey); Smaldon and Lyster, 1976
(Skarvoy: Norway; Crail, Kirkcudbrightshire: Scotland; Cornwall: England); Stubbings, 1965 (Hann,
Saloum River: Senegal); Stubbings, 1967 (Goree, Hann: Senegal); Utinomi, 1959 (Banyuls-sur-Mer:
France); Zakhama-Sraieb et al., 2010 (Gulf of Gabès: Mediterranean Sea).
15. A.3 INDO–WEST PACIFIC
Annandale, 1906 (Rameswaram Island: India; Gulf of Manaar); Balazs, 1978 (Hawaii); Balazs,
1980 (Hawaii); Balazs et al., 1987 (Hawaii); Borradaile, 1903 (Minikoi Island: India); Broch,
1916 (Broome: Australia); Broch, 1931 (Gulf of Thailand; Nagasaki: Japan); Broch, 1947
(Ream: Cambodia; Indochina); Bustard, 1976 (Great Barrier Reef: Australia); Daniel, 1956
(Tuticorin, Drusadai Islands, Royapuram Coast, Madras Coast: India); Daniel, 1962 (Little Andaman
412 The Biology of Sea Turtles, Volume III
Island: India); Darwin, 1854 (Low Archipelago: French Polynesia; Australia); Dawydoff, 1952 (Pulo
Condore: Vietnam; Ream: Cambodia); Deraniyagala, 1939 (Bentota: Ceylon); Dobbs and Landry,
2004 (Great Barrier Reef: Australia); Fernando, 1978 (Porto Novo: India); Glazebrook and Campbell,
1990 (Torres Strait: Australia); Fischer, 1886 (Pulo Condor: Vietnam); Foster, 1978 (North Island: New
Zealand); Frazier, 1971 (Aldabra Atoll); Frazier et al., 1985 (Orissa: India; Tanzania: Africa); Frazier,
1989 (Dwarka Island: India); Frazier et al., 1992 (Orissa, Gujarat: India; Karachi, Pakistan);Gordon,
1970 (Hawaii); Gruvel, 1903 (Seychelles; Mallicolo: Vanuatu; Djibouti; Sandwich Island; Cochinchina:
Vietnam); Gruvel, 1907 (Andaman Islands: India); Gruvel, 1912 (Tuamotu Archipelago: French
Polynesia); Hayashi and Tsuji, 2008 (Okinawa: Japan); Hendrickson, 1958 (Johor, Sarawak: Malaysia);
Hiro, 1936 (Wakayama Prefecture, Aichi Prefecture: Japan); Hiro, 1937a (Baberudaobu Island: Palau);
Hiro, 1939 (Toyama Bay: Japan); Jones, 1990 (Australia); Jones et al., 1990 (Tasmania; Australia);
Jones et al., 2000 (summary of distribution); Kruger, 1911b (Sagami Bay: Japan); Kruger, 1912 (Timor
Sea); Lanchester, 1902 (Kota Bharu: Malaysia); Limpus et al., 1983a (Campbell Island: Australia);
Limpus et al., 1983b (Crab Island: Australia); Limpus et al., 2005 (Raine Island: Australia); Loop
et al., 1995 (Milman Island: Australia); Losey et al., 1994 (Hawaii); Matsuura and Nakamura, 1993
(Kagoshima Prefecture: Japan); McCann, 1969 (North Island: New Zealand); Monroe and Limpus,
1979 (Queensland: Australia); Mustaquim and Javed, 1993 (Sandspit Beach: Pakistan); Newman et al.,
1969 (Hawaii); Newman and Abbott, 1980 (California); Nilsson-Cantell, 1921 (Western Australia:
Australia); Nilsson-Cantell, 1930a (Enoe Island: Malaysia); Nilsson-Cantell, 1932 (Bentota: Sri Lanka);
Nilsson-Cantell, 1937 (Singapore); Nilsson-Cantell, 1938 (Maldives; Kilakarai, Andaman Islands,
River Hooghly, mouth of Ganges: India); Pillai, 1958 (Quilon: India); Pilsbry, 1916 (Hawaii; Caroline
Islands; Ana: Japan; Saigon: Vietnam); Pilsbry, 1927 (Hawaii); Ren, 1980 (Xisha Islands); Ren, 1987
(China); Ross, 1981 (Oman); Smaldon and Lyster, 1976 (Kuala Lumpur: Malaysia); Tachikawa, 1995
(Japan); Utinomi, 1949 (Hakata Bay: Japan); Utinomi, 1958 (Sagami Bay: Japan); Utinomi, 1966
(Amakusa: Japan); Utinomi, 1969 (Kharg: Iran); Utinomi, 1950 (Tanabe Bay: Japan); Utinomi, 1970
(Hakui, Cape Kyoga-misaki, Kamo, Nezugaseki, Sado Island: Japan); Wagh and Bal, 1974 (Bombay:
India); Weltner, 1897 (Massaua: New Guinea; Torres Strait); Weltner, 1910 (Ile Europa); Zann and
Harker, 1978 (Queensland: Australia); Zardus and Balazs, 2007 (Hawaii).
15. A.4 EASTERN PACIFIC
Angulo-Lozano et al., 2007 (Sinaloa: Mexico); Beaumont et al., 2007 (Galapagos Islands: Ecuador);
Brown and Brown, 1995 (Peru); Darwin, 1854 (Mexico; Galapagos Islands: Ecuador); Frazier et al.,
1985 (Galapagos Islands: Ecuador); Frazier et al., 1992 (Santa Rosa: Ecuador); Frick et al., 2011a,b
(Baja California: Mexico; Eastern Tropical Pacic; Galapagos: Ecuador); Green, 1998 (Galapagos
Islands: Ecuador); Henry, 1941 (La Paz: Mexico); Henry, 1960 (Gulf of California, Guaymas: Mexico);
Hernandez-Vasquez and Valadez-Gonzalez, 1998 (Jalisco: Mexico); Hubbs, 1977 (California);
Kolosvary, 1943 (San Jose: Guatemala); Lazo-Wasem et al., 2011 (Jalisco: Mexico); MacDonald,
1929 (Cocos Island: Costa Rica); Newman et al., 1969 (Baja California: Mexico; Eastern Pacic);
Pilsbry, 1916 (Baja California: Mexico; Galapagos Islands: Ecuador); Ross and Newman, 1967 (Baja
California: Mexico); Stinson, 1984 (California); Vivaldo et al., 2006 (Michoacan, Oaxaca: Mexico);
Weltner, 1897 (western Mexico; California; Valparaiso: Chile); Young and Ross, 2000 (Sonora:
Mexico); Zullo, 1986 (Galapagos Islands: Ecuador); Zullo, 1991 (Galapagos Islands: Ecuador).
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... Because epibiosis necessitates ecological overlap between host turtles and "free living" populations of epibionts and/or their propagules, the assemblages of epibionts found on sea turtles also tend to reflect the regions and habitats where host turtles spend time (e.g., Reich et al., 2010;Pfaller et al., 2014;Ten et al., 2019). Consequently, the presence of certain epibiont species or assemblages that occupy specific regions (e.g., tropical, temperate, or polar) and/or habitats (e.g., oceanic/pelagic or neritic/benthic) can serve as indicators of the migratory movements and habitat preferences of sea turtles (Casale et al., 2004;Frick and Pfaller, 2013). Similarly, the diversity of sea turtle epibionts and the equally diverse ways they interact with their hosts, means that the presence or absence of particular epibiont taxa can also serve as indicators of the hosts' foraging preferences (Pfaller et al., 2014), social or reproductive behavior Robinson et al., 2017a), body condition and/or health status (Lazo-Wasem et al., 2007;Nolte et al., 2020), and more. ...
... Following a rich history of anecdotal reports dating back to Darwin (1851Darwin ( , 1854 and Pilsbry (1916), the epibiont communities of sea turtles have received considerable attention (Frick and Pfaller, 2013). Most of this work has focused on animal, macro-epibionts (>1 mm) as they are relatively easy to identify and sample; however, it is increasingly being realized that sea turtles also frequently host meio-and micro-epibionts as well as various plant species (Robinson et al., 2016;Ingels et al., 2020). ...
... First, because epibiosis necessitates spatial overlap between the ranges of host turtles and their epibionts (Frick and Pfaller, 2013), sea turtle species with wider geographic ranges would theoretically encounter a greater diversity of potential epibionts and thus host greater richness and diversity. Consistent with this hypothesis, Kemp's ridleys and flatbacks have the smallest geographic ranges of the seven sea turtle species and host the lowest epibiont richness and diversity. ...
Article
Full-text available
Competition for space drives many marine propagules to colonize the external surfaces of other marine organisms, a phenomenon known as epibiosis. Epibiosis appears to be a universal phenomenon among sea turtles and an extensive body of scientific literature exists describing sea turtle-epibiont interactions. When viewed in isolation, however, these epibiont “species lists” provide limited insights into the factors driving patterns in taxonomic diversity on a global scale. We conducted an exhaustive literature review to collate information on sea turtle-epibiont interactions into a global database. As studies involving meio- and micro-epibionts, as well as plants, are limited, we exclusively focused on animal, macro-epibionts (>1 mm). We identified 304 studies that included a combined total of 1,717 sea turtle-epibiont interactions involving 374 unique epibiont taxa from 23 Higher Taxon categories (full Phylum or select phyla differentiated by Subphylum/Class/Subclass). We found that loggerhead turtles hosted the highest taxonomic richness (262 epibiont taxa) and diversity, including representative taxa from 21 Higher Taxon categories, followed by hawksbill, green, olive ridley, leatherback, Kemp’s ridley, and flatback turtles. In addition, the taxonomic richness for all turtle species except leatherbacks was projected to increase with additional studies. We found that taxonomic richness not only varies between species but also between well-studied populations of loggerhead turtles. Lastly, we assessed biases in the current literature and identified knowledge gaps for certain species (e.g., Kemp’s ridleys and flatbacks), life stages (e.g., juveniles), habitats (e.g., oceanic habitats), and geographic regions (e.g., central Pacific, east Atlantic, and east Indian oceans). Our hope is that this database will serve as a foundational platform for future studies investigating global patterns of the diversity, ecological function, and evolutionary origins of sea turtle epibiosis.
... Epibiosis is a symbiotic relationship where one organism (epibiont) lives on the surface of the other (basibiont) (Wahl and Mark, 1999;Harder, 2008). A wide variety of epibiont communities are found on sea turtles (Wahl, 1989;Pfaller et al., 2008b;Frick and Pfaller, 2013;Majewska et al., 2015) including macro, meio, and micro-epibionts. Macro-epibiont communities encompassing cirripeds, polychaetes, hydrozoans, bryozoans, poriferans, tunicates, periphytic algae, and some motile organisms have been widely studied on different sea turtle species (Caine, 1986;Pfaller et al., 2008b;Fuller et al., 2010;Lazo-Wasem et al., 2011;Robinson N. J. et al., 2017;Robinson et al., 2019), and meiofaunal organisms such as nematodes and copepods have recently been the focus of several studies (Aznar et al., 2010;Corrêa et al., 2013;Domènech et al., 2017;Ingels et al., 2020). ...
... Barnacles are the most prominent epibionts of sea turtles (Casale et al., 2012;Frick and Pfaller, 2013). Turtle barnacles belong to the superfamily Coronuloidea and include three families: Chelonibiidae Pilsbry, 1916, Coronulidae Leach, 1817, and Platylepadidae Newman and Ross, 1976 (Hayashi, 2012(Hayashi, , 2013. ...
... Epibiotic barnacles and crabs have also been used as indicators of the distribution and movement of loggerheads (Casale et al., 2004). Thus, epibiont communities could roughly reflect the environment in which the host has recently been living (Casale et al., 2012;Frick and Pfaller, 2013;Nolte et al., 2020;Silver-Gorges et al., 2021). In addition, this method could be very useful in sea turtle conservation planning efforts, as epibionts may affect their health status. ...
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Sea turtle epibionts can provide insights into the hosts' habitat use. However, at present, there is a lack of information on sea turtle epibiont communities in many locations worldwide. Here, we describe the epibiont communities of 46 hawksbill turtles (Eretmochelys imbricata) in the Persian Gulf. Specifically, we sampled 28 turtles from the Dayyer-Nakhiloo National Park (DNNP) in the northern Gulf and 18 turtles from Shibderaz beach in the Strait of Hormuz. A total of 54 macro, meio, and micro-epibiont taxa were identified, including 46 taxa from Shibderaz and 29 taxa from DNNP. The barnacles Chelonibia testudinaria and Platylepas hexastylos, as well as harpacticoid copepods and Rotaliid foraminifers, had the highest frequency of occurrence found on almost all turtle individuals. Harpacticoids were the most abundant epizoic taxa (19.55 ± 3.9 ind. per 9 cm 2) followed by forams (Quinqueloculina spp.: 6.25 ± 1.5 ind. per 9 cm 2 and Rotaliids: 6.02 ± 1.3 ind. per 9 cm 2). Our results showed significant differences between the study sites in the composition of micro and macro-epibiont communities found on hawksbill turtles. We speculate that the differences in epibiont communities were largely influenced by local environmental conditions.
... Stephanolepas mucricata is an encrusting balaniform barnacle. It usually attaches to the anterior edge of the anterior flippers of sea turtles but has been reported on sea snakes and fish (Frick & Pfaller, 2013). It is native to coastal-neritic regions of the Indo-Pacific (Jones et al., 2000). ...
... Stephanolepas mucricata, cirrípedo balaniforme incrustante, generalmente se adhieren en el borde anterior de las aletas anteriores de las tortugas marinas, también se han reportado en serpientes marinas y en peces (Frick & Pfaller, 2013). Es de origen nativo de regiones costero -neríticas del Indo -Pacifico (Jones et al., 2000). ...
... In Paracas, we observed Chelonibia testudinaria, Platylepas hexastylos, and Stephanolepas muricata, all of which are of coastal-neritic origin and generally associated with warm tropical or subtropical waters in the eastern Pacific (Jones et al., 2000;Bugoni et al., 2001;Gittings, 2009;Frick & Pfaller, 2013). The turtles with these epibionts showed a mean CCL of 58.2 cm (Fig. 8). ...
Article
Full-text available
RESUMEN Quiñones J, Quispe S, Romero C, Paredes E. 2021. Parámetros poblacionales y biológicos de la tortuga verde del Pacífico este, principal zona de reclutamiento en el Pacífico sur este. Bol Inst Mar Perú. 36(1): 106-130.-Con el objetivo de determinar los principales parámetros poblacionales de la tortuga verde del Pacifico este (Chelonia mydas agassizii) el Instituto del Mar del Perú (IMARPE), mediante el Laboratorio Costero de Pisco, a partir del 2010 empezó las investigaciones biológicas en tortugas marinas, a través de monitoreos acuáticos en la ensenada de la Aguada, en Bahía Paracas, Pisco. Durante el periodo 2010-2017 se determinó el largo curvo del caparazón (LCC), presentando promedio de 58,4 ± 7,9 cm (rango: 40,9-84,5 cm, n=438) con 88,7% de juveniles y 11,3% de sub-adultos. Estas tallas son las menores registradas en el Pacifico este para la especie. El número promedio de tortugas capturadas por km de red tendida por hora fue 1,03 ±1,23 (rango: 0-5,9, n=83). Los principales epibiontes capturados fueron de origen costero-nerítico: Platylepas hexastylos (40,5%, n=570), Stephanolepas muricata (13,4%, n=189), Conchoderma virgatum (13,1%, n=184), Ozobranchus margoi (12,9%, n=181), Chelonibia testudinaria (10,3%, n=145), y también de origen pelágico-oceánico: Lepas anatifera (8,5%, n=120), Planes cyaneus (0,8%, n=11) y Remora remora (0,6%, n=7). Se evidencia la gran importancia de Paracas como una exclusiva zona de reclutamiento desde zonas oceánicas. Durante lo que va del proyecto (2010-2017) se realizaron 46 recapturas, de las cuales 41 fueron juveniles y 5 sub-adultos, también se reportaron 5 triples recapturas (todos juveniles). La residencia en el área, expresada en el número promedio de días utilizados por la especie en el área de alimentación fue de 306,2 ± 166,9 días (rango: 170-708, n=26), la tasa de crecimiento fue de 7,4 ± 2,8 cm/año (rango: 2,0-11,7, n=26), ambos análisis se realizaron considerando recapturas mayores a 170 días. El índice de condición corporal (BCI) promedio por año y por estadio fue mayor en juveniles (1,49) con respecto a los sub-adultos (1,43). La mayoría de los parámetros poblacionales fueron favorables, las altas tasas de crecimiento y de BCI en conjunto con las bajas tasas de recapturas demuestran que esta es una población grande, saludable y con posibles bajos niveles de endogamia. Paradójicamente es preocupante que aun subsistan capturas incidentales y dirigidas en la zona, por lo que son necesarias y urgentes las medidas de conservación y fiscalización en la zona de Pisco-Paracas. Palabras clave: Chelonia mydas agassizii, Paracas, parámetros poblacionales, tortuga verde del Pacifico esteú ABSTRACT Quiñones J, Quispe S, Romero C, Paredes E. 2021. Biological and population parameters of the green sea turtle Chelonia mydas agassizii in Paracas-Pisco, the main recruitment area in the Southeast Pacific. Bol Inst Mar Peru. 36(1): 106-130.-In 2010, the Instituto del Mar del Peru (IMARPE), via the Coastal Laboratory of Pisco, began biological research on sea turtles to determine the main population parameters of the green sea turtle (Chelonia mydas agassizii), through aquatic monitoring in the Aguada inlet, located in Paracas Bay, Pisco. Between 2010 and 2017, the curved carapace length (CCL) was determined, showing a mean of 58.4 ± 7.9 cm (range: 40.9-84.5 cm, n=438) with 88.7% of juveniles and 11.3% of sub-adults. These sizes are the smallest recorded in the eastern Pacific for the species. The mean number of turtles caught per km of net set per hour was 1.03 ±1.23 (range: 0-5.9, n=83). The coastal-neritic epibionts caught were Platylepas hexastylos (40.5%, n=570), Stephanolepas muricata (13.4%, n=189), Conchoderma virgatum (13.1%, n=184), Ozobranchus margoi (12.9%, n=181), Chelonibia testudinaria (10.3%, n=145), and those of pelagic-oceanic origin were: Lepas anatifera (8.5%, n=120), Planes cyaneus (0.8%, n=11), and Remora remora (0.6%, n=7), thus evidencing the great importance of the area and one of the most important recruitment areas of the eastern Pacific. So far in the project (2010-2017), we have made 46 recaptures, of which 41 were juveniles and 5 sub-adults, plus 5 triple recaptures (all juveniles). So far in the project (2010-2017), we have made 46 recaptures, of which 41 were juveniles and 5 sub-adults, plus 5 triple recaptures (all juveniles). Residence in the area, expressed as the mean number of days used by the species in the feeding area was 306.2 ± 166.9 days (range: 170-708, n=26), the growth rate was 7.4 ± 2.8 cm/year (range: 2.0-11.7, n=26), both analyses were performed by considering recaptures greater than
... The analysis of epibiota on sea turtle carapaces offers great potential for the study of the turtle behavior, diet, foraging locations, migration routes and biogeography (Robinson et al. 2016, Majewska et al. 2017, Van de Vijver et al. 2020). Although a large number of studies focused on macro-epibiota and the effect of their associations with the host organisms (Schwartz et al. 1978, Frazier et al. 1985, Frick & Pfaller 2013, Robinson et al. 2017, there is a growing interest in the role and diversity of micro-epibiota attached to sea turtles (Ingels et al. 2020) with a recent steep increase in publications reporting on epizoic diatoms associated with sea turtles (Frankovich et al. 2015, Majewska et al. 2015, Robinson et al. 2016, Majewska et al. 2017, Majewska et al. 2019. Apart of diatoms, large clumps of other periphytic micro-and macroalgae, including Cyanophyceae, Chlorophyceae, Alveolatae, Phaeophyceae and Rhodophyceae were reported to grow on the carapace of sea turtles (Frick 1998, Sentíes et al. 1999). ...
... The loggerhead sea turtles, known to be omnivorous using both oceanic and coastal foraging habitats, host the highest diversity of micro-epibionts (Pfaller et al. 2008, Ingels et al. 2020. A necessary prerequisite for epibiosis is a geographic and ecological overlap between the host and the epibiont (Frick & Pfaller 2013). This may explain why all species of diatoms diatom reported from loggerhead sea turtle carapaces show a preference for benthic habitats (Van de Vijver et al. 2020, Kaleli et al. 2020). ...
Article
Chrysophyte algae live predominantly in freshwater habitats, therefore marine chryso-phyte stomatocysts are less common and poorly documented. Here we report on the occurrence of two unknown chrysophycean stomatocysts in a complex epizoic biofilm formed on a carapace of a loggerhead sea turtle (Caretta caretta) found injured on the southeastern coast of the Adriatic Sea and admitted to the Sea Turtle Rescue Centre in Aquarium Pula, Croatia. Stomatocyst #1 is characterized by a thickened circulus giving the cyst an asymmetrical outlook whereas stomatocyst #2 has a thick, wide, irregularly shaped collar. Detailed morphological investigations based on scanning electron microscopy observations and comparison with known chrysophyte stomatocysts worldwide , showed that both should be described as new to science following the guidelines of the International Statospore Working Group (ISWG).
... taxonomically diverse macro-epibionts, including barnacles, amphipods and red algae (Hollenberg, 1971; 75 Broderick et al., 2002;Frick and Pfaller, 2013). Some of these organisms require the sea turtle 76 substratum to attach and thrive, and thus their survival is inextricably linked to the wellbeing and fitness 77 In the present study we decided to further expand the perspective and study the whole 96 microbial community found on external surfaces of loggerhead sea turtles from the Mediterranean Sea. ...
Preprint
Loggerhead sea turtle is considered a keystone species with major ecological role in Mediterranean marine environment. As with other wild reptiles, their outer microbiome is rarely studied. Although there are several studies on sea turtle's macro-epibionts and endo-microbiota, there has been little research on epibiotic microbiota associated with sea turtles' skin and carapace. Therefore, we provide the first identification of combined epibiotic eukaryotic and prokaryotic microbiota on Mediterranean loggerhead sea turtles. In this study, we sampled skin and carapace of 26 loggerheads from the Mediterranean Sea during 2018 and 2019. To investigate the overall microbial diversity and composition, amplicon sequencing of 16S and 18S rRNA genes was performed. We found that the Mediterranean loggerhead sea turtle epibiotic microbiota is a reservoir of a vast variety of microbial species. Microbial communities between samples mostly varied by different locations and seas, while within prokaryotic communities' significant difference was observed between sampled body sites (carapace vs. skin). In terms of relative abundance, Proteobacteria and Bacteroidota were the most represented phyla within prokaryotes, while Alveolata and Stramenopiles thrived among eukaryotes. This study, besides providing a first survey of microbial eukaryotes on loggerheads via metabarcoding, identifies fine differences within both prokaryotic and eukaryotic microbial communities that seem to reflect the host anatomy and habitat. Multi-domain epi-microbiome surveys provide additional layers of information that are complementary with previous morphological studies and enable better understanding of the biology and ecology of these vulnerable marine reptiles.
... Excessive epibiont load is probably a consequence of the turtle's inability to access cleaning stations to control them (Losey et al., 1994). On the other hand, the lower epibiotic load found in SC turtles may be related to a less favorable habitat, causing the death of the less tolerant epibionts (Frick and Pfaller, 2013). ...
Article
In 2015, the failure of the Fundão dam caused the release of 43 million m³ of tailings into the Doce River Basin, in southeast Brazil. It was considered the largest environmental disaster of the world mining industry. The tailings, composed mostly of heavy metals, caused massive destruction of the Doce River ecosystem endangering the organisms that live in the coastal zone where the mud reached the ocean. Among the exposed species are the sea turtles that use the region for food. The aim of this study was to evaluate the effect of contaminants on the health status of juvenile green sea turtles that feed in a coastal area exposed to ore mud (Santa Cruz) and to compare them with animals from an area not directly affected (Coroa Vermelha). A physical examination was performed to determine the health status. Blood samples were analyzed for hematological and biochemical parameters, and metal concentrations (As, Cd, Cr, Cu, Fe, Hg, Mn, Pb, and Zn). Santa Cruz sea turtles had more ectoparasites and a higher incidence of fibropapillomatosis. Statistically significant differences between sites were found for levels of calcium, phosphorus, glucose, protein, albumin, globulin, cholesterol, triglycerides, urea, CPK, ALT, and AST. The count of leukocytes, thrombocytes, and heterophils, as well as the concentrations of As and Cu were higher in Santa Cruz turtles. Together the results show a worse nutritional status and a greater degree of liver and kidney damage in animals affected by the tailings. The health status may indicate a physiological deficit that can affect their immune system and behavior, which is supported by the higher fibropapillomatosis tumor score and ectoparasite load in these animals. These results support the need for long-term monitoring of the exposed area to quantify the direct and indirect influence of the heavy metals levels on sea turtles and how this reflects the environmental health.
... Many studies have created lists of epibionts that have been identified on different hosts [2,3]. The body surface of sea turtles is often used by epibiont fauna as a settlement substrate and as a means of dispersal and food procurement [4]. Analysis of epibionts may provide information on sea turtle biology and ecology, indicating types of environments passed through, migration times and depth, regional occurrence, habitat use, health, seasonality, behavior, gender-based patterns, and signs of climate change [5,6]. ...
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The present study contributes to the knowledge of epibionts recorded on sea turtles that nested on a beach in the South Pacific of Mexico. A total of 125 Lepidochelys olivacea turtles nested on Llano Real beach, Guerrero, Mexico, were examined. We collected 450 conspicuous organisms from 8 species from 43 turtles. The corresponding data analysis was carried out to obtain the relative abundance, the relationship between turtle sizes and the presence of organisms, the similarity of species between the sampling months, and the interspecific relationships between the epibionts and the turtles observed. Chelonibia testudinaria was the most abundant species, while Remora remora was the least abundant species. The turtles were divided into six body sections, with the greatest abundance of these organisms located in the head–neck section of turtles, and there was a significant difference in the size of the turtles that presented epibionts and those that did not. C. testudinaria showed greater similarity between sampling months, and the interspecific relationships recorded were commensalism, parasitism, amensalism, and protocooperation. This research contributes the first record of epibionts in L. olivacea nesting in Guerrero, Mexico.
Presentation
Xenobalanus globicipitis is an epibiont of cetaceans that typically attaches on the edge of fins. Recent evidence showed that its distribution on the tail flukes of striped dolphins, Stenella coeruleoalba, was non-random; most barnacles occurring on the dorsal side, and the central third, of the trailing edge of the flukes. These patterns were interpreted based on functional demands regarding barnacle structural integrity and/or filtering performance. The present study provides evidence that this seemingly preferential use of some fluke areas may actually be a consequence of dolphin hydrodynamics. We performed an analysis of the distribution and aggregation of X. globicipitis on the flukes of 55 Mediterranean striped dolphins, and interpreted the patterns obtained using published evidence on swimming dolphin models based on computational fluid dynamics. Nearest neighbor analysis strongly suggested that new barnacle recruits actively seek placements along the trailing edge beside already settled individuals, presumably to facilitate copulation. However, the gross distribution of X. globicipitis on the flukes was directly related with cetacean hydrodynamics, preferentially settling on areas of higher pressure and lower shear stress. Accordingly, these results suggest that X. globicipitis could be used as a natural tag to shed light on cetacean hydrodynamics.
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This study examines the barnacle symbionts on 168 blue crab both shallow and deep estuarine environments in the area of B pose of the study was to quantify the prevalence, intensity, a the ectosymbiotic barnacle Chelonibia patula on blue crabs. T was 67%. There was no difference in the prevalence of barna sus the deep environment. Results indicate female crabs were s This suggests that the prevalence and intensity of barnacles a gratory habits of the host, since female crabs spend more tim where they are more likely to be fouled by barnacle larvae. Th the crab carapaces was controlled by the surface topography o on the lateral regions than medial. The orientation of the carin the carapaces of the host crabs was measured, but no preferre and benefits of epibiosis are reviewed and the barnacle/blue c beneficial to the barnacles than to the host blue crabs.
Chapter
The closest interaction of an organism with its environment is the ingestion of a subset of that environment and the subsequent alteration and absorption of that subset as it passes through the digestive tract of the organism. The absorbed nutrients fuel the productivity — both growth and reproduction — of the organism. The pivotal 200role that nutrition plays in the productivity of individuals and populations — and thus to the conservation of species — has often been overlooked.