Size-dependent predation and intraspecific inhibition of an estuarine snail feeding on oysters

Predator outbreaks have increased in the past two decades in many ecosystems and are predicted to become more common with climate change. During these outbreaks, predator densities increase rapidly, and can cause large reductions in prey populations or shifts in prey size structure. However, unexpected interactions may occur at high predator densities, necessitating a mechanistic understanding of how increased predator density affects predator-prey dynamics. In the northern Gulf of Mexico, outbreaks of southern oyster drill (Stramonita haemastoma, Linnaeus, 1767) occur during high salinity events, and can greatly reduce eastern oyster (Crassostrea virginica, Gmelin, 1791) populations. A large outbreak of drills occurred from 2013—2015 in Apalachicola Bay, FL which corresponded with an oyster fishery collapse in that bay. To improve our mechanistic understanding of predation during such a high-density outbreak, laboratory experiments based on field observations were used to quantify the prey size selection by drills and the drill functional response, as a function of drill abundance. Drills fed on medium-sized oysters (50-75 mm) more often than small and larger-sized oysters, and often formed aggregations during feeding events. However, despite this aggregative response, there was a negative relationship between per capita feeding rates and drill abundance. Indeed, the Crowley-Martin functional response model had the most parsimonious fit to the data, suggesting that predator-predator inhibition reduced attack rates and increased handling times. Due to an increase in regional drought conditions and water usage in the southeastern United States, drill outbreaks will likely increase in frequency and duration. A greater understanding of how predation rates change with predator densities during outbreaks will improve predictions of oyster mortality, and strengthen the scientific framework for oyster fishery decisions.

Methods
This experiment used drills and oysters that were collected from subtidal habitats in Apalachicola Bay, FL USA (both collections occurred around 29º 40’ 32.56” N, 84º 51’ 36.76” W and 29º 42’ 7.2” N, 84º 49’ 31.76” W), and was carried out at the University of South Florida, College of Marine Science in St. Petersburg, FL (USFCMS). At USFCMS three separate, closed-seawater systems, each comprising ten experimental tanks (47.3 l; 68 ´ 40 ´ 27.5 cm), were constructed for a total of 30 tanks. The base area of these tanks was similar to the first experiment, 0.27 m2. Within each system, approximately 950 l of artificial seawater was recirculated through the experimental tanks and a large sump (633 l; 76 ´ 45.5 ´ 183 cm). In Experiment II at UFSCMS, salinity was maintained at 25 by mixing deionized water with Instant Ocean sea salt (Instant Ocean Spectrum Brands, Blacksburg, VA, USA), and checked daily with a YSI 85 (Xylem Inc, Yellow Springs, OH, USA). Water temperature was maintained between 20-22°C using Finnex TH-800 Plus, 800-watt titanium heating rods (Finnex, Chicago IL, USA) with a Reef Octopus Heater Controller (Honya Co. Ltd, Shenzhen, China). The temperature and salinity were chosen based on conditions that occurred during an outbreak in the northern GOM (Menzel et al.,1966; FFWCC, 2013). During both experiments and the one week holding prior to Experiment II, oysters were fed Instant Algae Shellfish Diet 1800 (Reed Mariculture Inc, San Jose, CA) daily, following the manufacturer’s instructions of 3.6 ml per 100 g of oyster wet weight.

In the seawater system at USFCMS, six drill abundances (2, 3, 4, 6, 8, and 12 drills per tank) were orthogonally crossed with five oyster abundances (3, 4, 6, 8, and 12 per tank), yielding two replicates for each orthogonal cross. The wide range of abundances reflects a response-surface approach to the regression analysis, improving the chances of detecting interactions between experimental factors despite low replication at any one combination of treatments. The treatment abundances were equivalent to densities ranging from 7-44 m-2 (drills) and 16-65 m-2 (oysters), both within the natural range observed for each species during and after outbreak conditions (See Supplemental Fig. 1). In this second experiment, drills ranged in size from 30-81 mm and were separated into small (30-55 mm) and large (56-81 mm) size classes. Oysters ranged in size from 25-99 mm and were separated into small (25-49 mm), medium (50-74 mm), and large (75-99 mm) size classes, as in Experiment I. Abundances of drills and oysters were split equally among each size class. To quantify oyster mortality in the absence of drills, each level of oyster abundance was paired with a corresponding control treatment (n=2) that lacked an oyster drill; no oysters died in these controls. After collection from the field, drills were held for one week and allowed to feed ad libitum on oysters before the start of the experiment to reduce any transportation effect to USFCMS from Apalachicola Bay, FL. The experiment began with a 5-day starvation period, based on the feeding rate of individual-housed drills from Experiment I, to standardize predator hunger. During feeding trials, tanks were checked twice daily for dead oysters, and the number of drills on each oyster was counted. Any dead oysters were replaced with a live oyster from the same size class to preserve a constant prey density, as assumed in predator functional response models that quantify the instantaneous feeding rate as opposed to the integrated feeding rate. After the 15-day experimental period, both the per capita feeding rate and the aggregate feeding rate (oysters consumed per replicate) were calculated.