DOI: 10.5061/dryad.mpg4f4qwf
title: Relationships between a common Caribbean corallivorous snail and protected area status, coral cover, and predator abundance

description: As coral populations decline across the Caribbean, it is becoming
 increasingly important to understand the forces that inhibit coral
 survivorship and recovery. Predation by corallivores, such as the short
 coral snail Coralliophila abbreviata,are one threat to the health
 of reefs worldwide, but understanding of the factors controlling
 corallivore populations, and therefore corallivore predation pressure,
 remains limited. To examine the extent to which bottom-up (i.e.,
 coral prey) and top-down (i.e., predators) forces relate to C.
 abbreviata distributions, we surveyed C.
 abbreviata abundance, percent coral cover, and the abundance of
 potential snail predators across six protected and six unprotected reefs
 in the Florida Keys. We found that C.
 abbreviata abundance was lower in protected areas, which
 had more diverse predator assemblages, and that across all sites snail
 abundance generally increased with coral cover. C.
 abbreviata abundance had strong, negative relationships
 with two gastropod predators in particular - the Caribbean spiny
 lobster (Panulirus argus) and the grunt black margate
 (Anisotremus surinamensis). Further, we found the size of C.
 abbreviata was also related to reef protection status, with
 larger C. abbreviata on average in protected
 areas, suggesting these gape-limited predators may alter size
 distributions by targeting small snails. Combined, these results provide
 preliminary evidence that marine protection in the Florida Keys may be a
 mechanism available to preserve critical trophic interactions that
 indirectly promote coral success via control of local populations of the
 common corallivore C. abbreviata.
description: Study design To examine how bottom-up and
 top-down factors are related to local abundances of <i>Coralliophila
 abbreviata</i>, we surveyed 12 coral reefs that spanned the reef
 tract of the Florida Keys National Marine Sanctuary, USA. Although all
 reefs within the sanctuary are protected by some level of regulation and
 management, our survey sites included 6 reefs specifically designated as
 no-take zones called Sanctuary Preservation Areas (hereafter called “SPAs”
 or “protected” sites) where fishing, harvesting, or possessing any marine
 life is prohibited (National Marine Sanctuaries 2015). Fishing is allowed
 within the other 6 non-SPA sites surveyed (hereafter called “non-SPAs or
 “unprotected” sites), which previous studies suggest have lower fish
 abundances than protected sites (Kramer and Heck 2007, Bartholomew et al.
 2008). All sites were part of the outer barrier reef system and surveys
 were conducted on the main portion of the shallow reef structure
 (&lt;30 meters in depth), including reef flats, edges, and spur and
 groove formations. All surveys were conducted between June – July
 2015. All survey methods were performed in accordance
 with relevant guidelines and regulations. The permit FKNMS-2015-064 was
 obtained from Florida Keys National Marine Sanctuary and the special
 activity license SAL-14-1580-SR was obtained from the Florida Fish and
 Wildlife Conservation Commission to conduct this research.
 Corallivore surveys Local abundances of
 <i>C.</i><i> abbreviata</i> were assessed using
 visual SCUBA surveys. At each site, two divers examined all living coral
 colonies located within 12-15, 20x2 m belt transects spaced approximately
 15 m apart for the presence and abundance of <i>C.
 abbreviata</i>. The exact number of transects surveyed varied based
 on the size of the site and logistical constraints. On every coral present
 within each transect, divers visually examined and inspected the margins
 between living coral tissue and dead coral skeleton or the seafloor for
 the presence of snails, as <i>C. abbreviata </i>often inhabit
 these margins (Miller 2001, Williams and Miller 2005, Shaver et al. 2017).
 Inspection included lightly touching the margins of dead coral skeleton or
 seafloor to feel for snails, as small tufts of algae can sometimes be
 mistaken for snails. All <i>C. abbreviata </i>were counted and
 removed, and most were transported to land for biometric measurements.
 Counts of snails<i> </i>were pooled for each site and
 standardized for the number of transects surveyed. On
 land, we measured <i>C. abbreviata</i> shell length, shell
 thickness, and live snail biomass (i.e., including shell). Shell length
 was measured as the distance from the apex of the shell to the bottom of
 the operculum, while shell thickness was measured as the thickness of the
 operculum’s outer lip 5 mm into the aperture. Both metrics were measured
 using digital calipers. Biomass of live snails was measured using a
 digital scale. Bottom-up factors: hard
 corals Relative percent coral cover measurements at
 each site were determined by collecting and analyzing benthic cover
 photos. To do this, we photographed 40, 0.5-m<sup>2</sup>
 plots located within 13-15, 20x1-m belt transects spaced at least 5 meters
 apart. The number of transects per site varied based on the size of the
 reef. All photos were taken at the same height above the seafloor using a
 PVC apparatus attached to an underwater camera that pointed at the
 seafloor. All photographs were analyzed for the percent cover and
 abundance of all coral species using Microsoft Powerpoint and Excel 2016
 software with 25 random points on each slide to identify coral species and
 estimate cover. Each point was coded to the species level for corals. If
 points fell on top of objects that were above the seafloor (e.g., queen
 conch shells), points were moved to the closest area showing benthic
 cover. Top-down factors: predators
 To examine how much of the variation in <i>C. abbreviata
 </i>abundance could be explained by predator abundance, we conducted
 surveys of known gastropod-consuming fishes and other suspected predators
 of <i>C. abbreviata </i>(Baums et al. 2003a, Johnston and
 Miller 2006, Humann and Deloach 2014), as actual data on of <i>C.
 abbreviata</i> predators are limited (Baums et al. 2003b, Johnston
 and Miller 2006). We used existing scientific literature and books (Claro
 2001) to identify potential predators if they met one of three
 requirements: (1) previous research suggested they may be <i>C.
 abbreviata</i> predators, (2) they had been observed preying on
 <i>Coralliophila</i> spp., or (3) they were taxa that
 specialize in feeding on gastropods. The following species were thus
 included in surveys as potential <i>C. abbreviata</i>
 predators: Caribbean spiny lobster (<i>Panulirus argus</i>:
 Baums et al. 2003a, Humann and Deloach 2014), Family Labridae: slippery
 dick (<i>Halichoeres bivittatus</i>: Randall 1967),
 puddingwife (<i>Halichoeres radiatus</i>: Randall 1967),
 hogfish (<i>Lachnolaimus maximus</i>: Randall 1967, Baums et
 al. 2003a), Spanish hogfish (<i>Bodianus rufus</i>: Randall
 1967); Family Haemulidae: white grunt (<i>Haemulon
 plumineri</i>: Randall 1967), bluestriped grunt (<i>Haemulon
 sciurus</i>: Randall 1967), Caesar grunt (<i>Haemulon
 carbonarium</i>: Randall 1967), Spanish grunt (<i>Haemulon
 macrostomum</i>: Randall 1967), sailor’s choice (<i>Haemulon
 parra</i>: Randall 1967), porkfish (<i>Anisotremus
 virginicuss</i>: Randall 1967), black margate (<i>Anisotremus
 surinamensis</i>: Randall 1967); and Family Diodontidae:
 porcupinefish (<i>Diodon hystrixs</i>: Randall 1967: Randall
 1967). Queen triggerfish (Family Balistidae, <i>Balistes
 vetulas</i>: Randall 1967) and balloonfish (Family Diodontidae,
 <i>Diodon holocanthus</i>: Randall 1967) were also surveyed
 but were not observed in any site and were therefore excluded from further
 analyses. Due to logistical constraints, we were restricted from surveying
 some cryptic species that have also been cited in the literature as
 potential <i>C. abbreviata</i>predators (e.g., octopi: Baums
 et al. 2003a; the snapping shrimp, <i>Synalpheus
 fritzmuelleri</i>: Goldberg 1971).
 Fish surveys were conducted using the Stationary Point Count
 method (Ayotte et al. 2011), where two divers are stationary along a
 30-meter transect at 7.5 and 22.5-meters and each surveys a 15-meter
 diameter circle over a given time interval. At each site, we conducted 10
 fish surveys spaced at least 20 meters apart, allowing for a 5-minute
 acclimation period after which all species identified as potential
 predators of <i>C. abbreviata</i> were counted for 5 minutes.
 Surveys of the spiny lobster <i>P. argus</i> were conducted
 using timed-diver survey methods, where 1-2 SCUBA divers systematically
 swam over the reef site (where fish and snail surveys were conducted) and
 all <i>P. argus</i> observed during a 1-hour total period were
 recorded. If there were multiple divers, the time was split accordingly.
 These surveys took place before the 2-day recreational “mini-season” for
 spiny lobster from 29-30 July 2015 to avoid artificial differences in
 lobster abundance within and outside of SPAs. Underwater visibility was
 consistently high during this time period, allowing divers to conduct a
 clear visual census in each survey area. All surveys were conducted during
 the day between 1000 hrs and 1600 hrs due to lack of resources for
 nighttime surveying. Statistical Analysis
 <i>Corallivore abundance as a function of protection, coral
 cover, and predator abundance - </i>To examine the role of both
 bottom-up (available coral food resources) and top-down (presence of
 predators) forces and the role of site protection status in affecting
 local <i>C. abbreviata</i> abundance, we created a general
 linear model with a negative binomial distribution to describe snail
 abundance with survey size as an offset using the R packages MASS
 and foreign. We used total relative coral cover and total
 abundance of all potential snail predators surveyed in these models. Total
 cover of all coral species was included in these models, as this survey
 and previous surveys in the same sites have observed
 <i>C. abbreviata</i> preying on a large variety of coral
 species, with very few coral species where <i>C.
 abbreviata</i> feeding has never been observed. A negative binomial
 distribution was used due to overdispersion with Poisson models. We used
 protection, coral cover, and predator abundance as fixed effects in the
 initial model and then created additional plausible models by removing
 parameters and adding potential two-way interactions, ultimately selecting
 the most parsimonious model with the lowest AIC value. All analyses were
 conducted in R version 4.0.0 with the tidyverse suite of packages
 (Wickham et al. 2019). <i>Corallivore
 size as a function of protection, coral cover, and predator abundance
 –</i> All biometric measurements taken of <i>C. abbreviata
 </i>(e.g., shell length, thickness, and live snail biomass) covaried
 to some degree, and therefore conducted further analyses using only
 measurements of snail shell length. This is consistent with previous
 studies examining the how different coral species prey affect <i>C.
 abbreviata </i>life history using measurements of size in shell
 length (Johnston and Miller 2007). Additionally, shell
 length is the measurement most likely to affect gape-limited gastropod
 predators. We examined the role of site protection, coral cover, and
 predator abundance on <i>C. abbreviata </i>size distributions
 using a general linear model with a Gaussian distribution and identity
 link to describe snail shell length. All variables were included as fixed
 effects in the initial snail shell length model. We then created alternate
 plausible models by removing parameters and adding potential two-way
 interactions, ultimately selecting the most parsimonious model with the
 lowest AIC value. <i>Predator abundance and
 species richness between protected and unprotected reefs </i>-We
 additionally examined whether there were alternative characteristics of
 the predator community that might be driving snail distributions in and
 out of protected areas. To test whether the abundance and species richness
 of potential <i>C. abbreviata </i>predators varied due to site
 protection status, we performed Welch two-sample t-tests with Shapiro
 tests to check for normality and F tests to check for equal variances.
 Predator abundance log-transformed to better meet assumptions of
 normality. <i>Corallivore abundance as a function
 of specific potential snail predators </i>- The predators surveyed
 were a group of species thought to be most likely to prey on <i>C.
 abbreviata</i>, and the identity of actual predators was therefore
 unknown. Given that the global models above assessed total predator
 abundance in each site and it is unlikely that all species surveyed are
 predators of <i>C. abbreviata</i>, and that a major goal of
 this study was to identify <i>C. abbreviata </i>predators, we
 examined whether <i>C. abbreviata </i>abundance appeared to be
 related to any of the potential predator species surveyed. To examine
 these relationships, we created general linear models with negative
 binomial distributions to describe snail abundance as a function of each
 species’ abundance with survey size (for snail surveys) as an offset. A
 Bonferroni correction was applied to adjust for multiple comparisons of
 individual predator species (n=13), with a new alpha value of
 <i>P</i> &lt; 0.0038.