Introduction
Within an ecosystem, sympatric species can co-occur largely due to
ecological adaptations that reduce competition for resources and habitat
predation risk (Grether et al. 2017, Lankau 2011, Perri and Randall
1999, Siepielski and McPeek 2010, Zhao et al. 2020). The resulting
community structure, where a collection of species fills a variety of
ecological niches, is one that is fundamental to ecosystem functioning
(Genung et al. 2020, Petchey et al. 1999, Spaak et al. 2017). However,
shifts in environmental conditions can cause changes in these dynamics
and disrupt the overall ecosystem structure, potentially altering key
environmental functions or services. Generally, those niches with lower
functional redundancy are less resilient to change (Bellwood et al.
2003, reviewed by Biggs et al. 2020, Micheli and Halpern 2005). For
example, in African savannahs, the exclusion of even one of the primary
consumers of invasive and problematic shrub (Solanum
campylacanthum ) led to increases in its abundance (Pringle et al.
2014). S. campylacanhum is toxic to livestock and has negative impacts
on grazing species as well as vegetation (Pringle et al. 2014). Even
though three herbivorous species are known to forage in the understory
where the shrub grows, they function as complementary rather than
redundant consumers.
Ecological specialists differ from generalists in their overall niche
width (Clavel et al. 2010, Futuyma and Moreno 1988). That is,
specialists occupy a narrower niche, typically with regard to some
combination of habitat choice and food preference (Futuyma and Moreno
1988). Specialists have generally evolved to outcompete generalists,
maximizing the exploitation of the selected resource. They thrive when
environmental conditions are stable but can struggle to adapt in
variable conditions (Scheiner 2002). Examples of the vulnerability of
specialists to environmental perturbations exist throughout the fossil
record (McKinney 1997) and modern-day specialists are similarly
susceptible (Fourcade et al. 2021, Norden et al. 2013). The flexibility
of generalists makes them more resilient to change, but the
effectiveness of specialists makes them more difficult to replace.
However, with enough functional redundancy, it is possible for multiple
species of generalists to maintain an ecosystem service. For example,
Memmott et al. (2007) showed that while specialist pollinators were more
vulnerable to extinction, the network of resilient generalist
pollinators is sufficient to sustain plant populations.
Grooming behaviors are common in terrestrial organisms, having been
reported for mammals (Heine et al. 2017, Mooring et al. 2004), birds
(Cox 2012, Goodman et al. 2020), and arthropods (El-Awami and Dent 1995,
Invernizzi et al. 2015). These behaviors typically present in the form
of autogrooming (grooming oneself), or social grooming (typically
between conspecifics), and have two potential functions. First, the
removal of parasites from the body of the client reduces the direct
impacts of the parasites on the host and may also reduce the overall
abundance of the parasites. Grooming can have a secondary effect of
maintaining overall hygiene of external body surfaces, facilitating
social interaction, and/or reducing stress (Soares et al. 2011).
Grooming of heterospecifics is rare in terrestrial systems and is
limited primarily to generalists such as arthropod-feeding birds that
will opportunistically eat insects and arachnids from the bodies of
other animals (Samish and Rehacek 1999). The only apparent
interspecific-grooming specialists in terrestrial systems are the two
species in the family Buphagidae (oxpeckers, Bezuidenhout and
Stutterheim 1980). In contrast to terrestrial species, intraspecific
grooming is uncommon in marine organisms, having been reported for a
small number of fish species (Clague et al. 2011, Sikkel 1986, Sikkel
and Smit 2018). However, interspecific grooming, commonly referred to as
“cleaning”, is well documented and is especially common in shallow
reef systems.
In interspecific cleaning, certain fish or invertebrate species will
obtain most of their dietary requirements by gleaning ectoparasites off
other species of fishes. These interspecific mutualisms have evolved
more than once in small, “picker-type”, fishes and in some shrimps
(Vaughan et al. 2016). Cleaning interactions are of sufficient
importance to individual “client” or “host” fishes that such fishes
will interrupt other, biologically important activities (such as
spawning) to get cleaned (Cheney and Côté 2003, Poulin and Grutter 1996,
Sikkel et al. 2005). Within the many fish species that have evolved
cleaning behaviors, most are “facultative” cleaners that clean
occasionally or during specific life history stages but are overall not
heavily dependent on consumption of external parasites. Examples of
these include Thalassoma bifasciatum in the Caribbean (Dunkley et
al. 2018, Feddern 1965, Itzkowitz 1979, Losey 1974), Coris julisin the Mediterranean (Zander and Sotje 2002), and Johnrandallia
nigrirostris, in the Pacific (Quimbayo et al. 2017). Unique to coral
reef systems, there are also obligate (or “dedicated”) cleaning
specialists that rely primarily on the ectoparasites of client fishes as
their main food source. (Vaughn et al. 2016). This group includes
several species of Elacatinus gobies on coral reefs in the
Caribbean region (Arnal and Côté 2000, Côté et al. 1998, Côté and Soares
2011) and Labroides wrasses on coral reefs in the Indo-Pacific
(Côté and Brandl 2021, Grutter 1997a, Grutter 1997b, Losey 1972).
Whereas wrasses tend to wander (even if associated with a “cleaning
station”), cleaner gobies are often tightly associated with large
boulder corals where they sit and await clients (Losey 1974, Whittey et
al. 2021). While facultative cleaners tend to interact with a narrower
diversity of client species compared to dedicated cleaners, they can at
times eat a similar number of parasites (Grutter and Feeney 2016,
Narvaez et al. 2015).
Cleaners provide numerous benefits to both individual clients and the
overall community. Client-level effects of cleaners include facilitating
wound healing (Foster 1985), reduced stress (Bshary et al. 2007, Soares
et al. 2011), a decreased reliance on immune function (Ros et al. 2011),
and increased client growth rates (Waldie et al. 2011). At the community
level, the presence of cleaners impacts coral reef communities by
locally increasing species richness and abundance (Bshary 2003, Grutter
et al. 2003, Waldie et al. 2011). Among the myriad of services they
provide, cleaners are best known for feeding on, and thus, removing the
ectoparasites of client fishes. Although they consume several types of
ectoparasites, the primary diet of cleaner fishes consists of gnathiid
isopods (Arnal and Côté 2000, Grutter 1997a, Grutter and Feeney 2016,
Losey 1974, Sikkel et al. 2004, Vaughan et al. 2016) and cleaning
activity can significantly reduce gnathiid populations (Grutter et al.
2018).
Gnathiid isopods (“gnathiids”) are hematophagous arthropods that spend
the majority of their lives in the benthic substrate but emerge to feed
on a fish host (Sikkel and Welicky 2019, Smit and Davies 2004). As the
primary “broker” of cleaner-client interactions they can impact hosts
in multiple ways. These include influencing host behaviors such as
spawning (Sikkel et al. 2005), and migration (Sikkel et al. 2017), as
well as interactions between clients and cleaners (Grutter 2001, Sikkel
et al. 2004), reducing hematocrit (Jones and Grutter 2005), increasing
stress hormones (Triki et al. 2016), reducing juvenile fitness (Allan et
al. 2021, Sellers et al. 2019), and killing the host (Artim et al. 2015,
Hayes et al. 2011, Penfold et al. 2008, Sellers et al. 2019).
Consequently, gnathiids can negatively affect host populations (Hayes et
al. 2011, Penfold et al. 2008) and thus impact community dynamics (Coile
and Sikkel 2013, Grutter et al. 2018, Sikkel and Welicky 2019).
Gnathiids are most active during crepuscular and nocturnal periods
(Grutter 1999, Santos and Sikkel 2017, Sikkel et al. 2006) and will
parasitize a wide range of fish species (Coile and Sikkel 2013, Hendrick
et al. 2019, Jones et al. 2007, Nagel and Grutter 2007, Santos and
Sikkel 2017, reviewed by Sikkel and Welicky 2019). They attach to hosts
only temporarily (up to several hours for most species) to feed, but
once engorged with blood/body fluids, they return to the benthos to
digest and molt. Thus, gnathiids spend most of their life free-living
(Smit and Davies 2004, Tanaka 2007). Because of this unusual lifecycle,
they have been referred to variously as temporary ectoparasites,
protelean parasites, and micropredators.
There are several methods by which external parasites are consumed that
do not involve grooming but still impact the parasite burden of hosts by
reducing parasite population densities (reviewed by Johnson et al.
2010). This includes concomitant predation as well as predation of
free-living stages (Artim et al. 2017, Kaplan et al. 2009, Thieltges et
al. 2013). Because gnathiids spend most of their lives not associated
with a host, they are susceptible to
consumption
by many fish species, including the up to 70% of species that consume
invertebrates (Kramer et al. 2015). However, only one study, on a few
nocturnal carnivores, has examined consumption by non-cleaners. (Artim
et al. 2017).
Tropical western Atlantic coral reefs possess little functional
redundancy of cleaners, and dedicated cleaner fish provide an apparently
unique and critical ecosystem service that may not be compensated for
were they to suffer declines in abundance. Even dedicated invertebrate
cleaners are unlikely to provide sufficient compensation in the absence
of dedicated cleaner fish. For example, Ancylomenes pedersoni(Pederson’s cleaner shrimp), are dependent on the short-lived,Bartholomea annulata (corkscrew anemone, Huebner and Chadwick
2012, O’Reilly et al. 2018, Titus et al. 2017) that are patchy in their
distribution.
In contrast to the mostly nocturnal gnathiids, the dedicated cleaners
that are considered their primary consumers are diurnal, consuming them
only off the hosts’ body, and most active at dawn (Côté and Molloy 2003,
Grutter 1999, Pierera et al. 2022, Sazima et al. 2000, Sikkel et al.
2004). When determining functional redundancy, we must therefore widen
the scope beyond dedicated cleaners to consider the degree to which
facultative cleaner species and non-cleaners might provide additional
sources of gnathiid consumption. The main goal of this study was,
therefore, to test predictions of the hypothesis that coral reefs
possess a sufficiently high level of functional redundancy of gnathiid
consumption through some combination of facultative cleaners and
additional functional groups of non-cleaner fishes that consume
free-living gnathiids. Specifically, we tested whether: 1) other fish
functional groups consume significant numbers of free-living stages of
gnathiids and 2) whether consumption by facultative cleaners is
comparable to dedicated cleaners on Caribbean coral reefs. We
accomplished this by sampling gut contents from 61 reef fish species
from 16 families, representing multiple feeding guilds, collected across
three sites in the northeastern Caribbean.