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It Takes Guts to Locate Elusive Crustacean Prey

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It Takes Guts to Locate Elusive Crustacean Prey Vol. 538: 1–12, 2015 MARINE ECOLOGY PROGRESS SERIES Published October 28 doi: 10.3354/meps11481 Mar Ecol Prog Ser OPENPEN ACCESSCCESS FEATURE ARTICLE It takes guts to locate elusive crustacean prey R. S. Lasley-Rasher1,*, D. C. Brady1, B. E. Smith2, P. A. Jumars1 1University of Maine, Darling Marine Center, Walpole, ME 04573, USA 2NOAA, National Marine Fisheries Service, Northeast Fisheries Science Center, 166 Water Street, Woods Hole, MA 02543, USA ABSTRACT: Mobile crustacean prey, i.e. crangonid, euphausiid, mysid, and pandalid shrimp, are vital links in marine food webs. Their intermediate sizes and characteristic caridoid escape responses lead to chronic underestimation when sampling at large spa- tial scales with either plankton nets or large trawl nets. Here, as discrete sampling units, we utilized in- dividual fish diets (i.e. fish biosamplers) collected by the US National Marine Fisheries Service and North- east Fisheries Science Center to examine abundance and location of these prey families over large spatial and temporal scales in the northeastern US shelf large ecosystem. We found these prey families to be impor- tant to a wide variety of both juvenile and adult dem- ersal fishes from Cape Hatteras to the Scotian Shelf. Fish biosamplers further revealed significant spatial shifts in prey in early spring. Distributions of mysids and crangonids in fish diets shoaled significantly from NOAA scientist displaying a ‘shrimp-sampling device’: a February to March. Distributions of euphausiids and goose fish Lophius americanus caught by the Northeast Fish- eries Science Center Trawl Survey. pandalids in fish diets shifted northward during Photo: Anne Byford March. Of multiple hypotheses for these shifts, prey migration is most strongly supported. Rather than only the classic ontogenetic shift from feeding on shrimp to piscivory, of the 25 identified diet shifts in fish predators, 12 shifts were toward increased shrimp limited to large trawl nets and small plankton sam- feeding frequency with increasing body length. pling devices. Overlap between these tools is imper- fect, and some prey species vital to marine food webs KEY WORDS: Fish feeding · Northwest Atlantic · are sampled ineffectively. Caridoid or ‘shrimp-like’ Pandalidae · Mysidae · Euphausiidae · Crangonidae · crustaceans such as members of the families Crango- Migration nidae, Pandalidae, Mysidae and Euphausiidae can be easily missed or grossly underestimated with these common sampling techniques. INTRODUCTION Most crustaceans belonging to these groups are too small to be effectively sampled by large trawl nets The ability to understand ecological roles of impor- with mesh and liner openings of approximately 10 tant prey species at large spatial scales relies heavily and 1.25 cm, respectively (NEFC 1988). Furthermore, on the observational tools in use. In the northeastern standard plankton nets are usually towed quite slowly, US shelf large ecosystem (NESLE), tools used to sam- approximately 1 to 2 knots or 2 to 4 km h−1 (UNESCO ple organisms at the scale of 100s of km are primarily 1968), and the ‘caridoid escape responses’ exhibited © The authors 2015. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 2 Mar Ecol Prog Ser 538: 1–12, 2015 by these organisms allow them to evade nets in many standing of their large-scale distribution patterns will cases (Fleminger & Clutter 1975). Some species form fill knowledge gaps and may be useful in predicting dense schools or swarms that are patchily distributed effects of global stressors on their distributions and (Mauchline 1980), and often individuals occur within abundances. a few meters of the substratum during the day (Hurl- Here we utilize a long-term diet study conducted burt 1957, Haynes & Wigley 1969, Brown et al. 2005, by National Marine Fisheries Service (NMFS) and Sato & Jumars 2008), below the area swept by most Northeast Fisheries Science Center (NEFSC) to de - plankton sampling devices (Hardy 1926, UNESCO termine the occurrence of our 4 target prey families 1968, Reid et al. 2003). Sled samplers that are towed in the diets of fishes in the NESLE. Using gut con- faster more effectively sample epibenthic organisms tents of individual fishes as the sampling unit (i.e. a but are often tailored to a given bottom type or habi- fish biosampler) has been an effective tool for survey- tat, making comparisons difficult (Hessler & Sanders ing prey distribution. This technique has been ap - 1967). Their filling with sediments further under- plied to a diverse array of prey species, from isopods mines reliable quantitative estimates of abundance. (Rachlin & Warkentine 1997) to ctenophores (Link & Additionally, sediment-containing samples are more Ford 2006), and has been used to measure benthic logistically cumbersome and time consuming and species richness (Frid & Hall 1999, Link 2004). Fur- therefore less commonly used over large spatial scales ther, this approach has been used to sample capelin (but see Wigley & Burns 1971, Theroux & Wigley 1998). through cod diet analysis (Fahrig et al. 1993) and to Although information on broad-scale distribution detect effects of mobile bottom fishing gear (Smith et patterns of these taxa may be limited, regional and al. 2013). For each prey family we asked the follow- local studies consistently indicate that they are im - ing questions. (1) How important are these families to portant prey for many commercially important fishes fish species of the NESLE? (2) Is there a fish size and for baleen whales in the northwest Atlantic. threshold above which they are no longer eaten? Crangonidae are important prey organisms in adult Finally, (3) Can this sampling method resolve known flounder diets and also important predators of larval or putative patterns in the seasonal distribution of flounder (Witting & Able 1995). Euphausiidae domi- these shrimp? nate diets of whales (Ryan et al. 2014) and are impor- tant diet items of migrating salmon smolts in estuary mouths (Renkawitz & Sheehan 2011). Pandalidae METHODS include the commercially important north ern shrimp Pandalus borealis, which has experienced record low Fish collection numbers recently in the Gulf of Maine, resulting in fishery closures. P. borealis is also a major diet spe- Fish used for diet analysis were collected as part cies for commercially important fishes such as cod of the seasonal bottom trawl survey conducted by and is subjected to top-down control by cod preda- NEFSC. This survey uses a stratified random sam- tion (Worm & Myers 2003). Finally, Mysidae domi- pling design and samples depths from 8 to 400 m nate diets of cod <10 cm long (Link & Garrison 2002) (Azarovitz 1981, NEFC 1988). Each survey samples and serve as prey for adults and juveniles of other between 350 and 400 stations on the continental shelf commercially important species (Grecay & Targett between Cape Hatteras, NC, USA and Nova Scotia, 1996, Buchheister & Latour 2011). Canada, and lasts approximately 8 to 10 wk. Further These families perform additional vital ecosystem details are given in Azarovitz (1981) and NEFC (1988). functions. They are highly omnivorous, with most species feeding on phytoplankton, holo- and mero- zooplankton, as well as benthos. Some Mysidae Diet analysis can digest detritus, including cellulose (Zagursky & Feller 1985, Friesen et al. 1986). This high degree of Specific information regarding food-habits sam- trophic connectivity, coupled with extensive mobility, pling and data for the NESLE can be found in Link means that they play an important role in nutrient & Almeida (2000) and Smith & Link (2010). To sum- import and export through spatially decoupled forag- marize, a subset of collected fish species was ana- ing, somatic growth and excretion (Steinberg et al. lyzed for food habits from 1973 to present. From 1973− 2002, Jumars 2007). Given their obvious importance 1981, stomach contents were preserved and returned in marine food webs at regional scales, particularly to the laboratory for identification, and organisms for the NESLE (Smith & Link 2010), added under- were identified to the lowest possible taxon (often to Lasley-Rasher et al.: Locating elusive crustacean prey 3 species). From 1981−present, stomach contents were also affected by uncontrolled physiological variables, examined at sea. Approximately 25 to 40% of the such as tem perature effects on ingestion and diges- fish stomachs were empty, varying by species (Link tion. To determine the importance of each prey family & Almeida 2000). Surveys from 1973−2012 were con- in the diet of a given predator species, we calculated ducted in autumn and spring. Winter trawls were S conducted in 1978 and 1992−2007. Summer trawls P = ijr ijr S were conducted 1977−1981 and 1991−1995 (see ir Table S1 in the Supplement at www.int-res.com/ Where Pijr is the proportion of prey j in predator i articles/suppl/m538p001_supp.pdf). stomachs in region r. Sijr is the number of i predator stomachs containing prey j in region r. Sir is the total number of stomachs sampled for predator i in region Prey family importance r (including empty stomachs). We report diet propor- tions for the top 10 fish predators of each prey family, Given the changes in prey identification methods which correspond to species where prey of interest and species resolution over the time span of the sur- are found in at least 5% of the diets analyzed. vey, we chose to group shrimp by family (Table S2 in the Supplement). The total number of fish stomachs containing each prey family was compiled. These val- Statistical analysis ues are affected by en counter rates between predators and prey, predator preference, and also the numbers Statistical tests were conducted using Matlab of predator individuals sampled, which is unequal R2014b and R (R Core Development Team 2009). among predator and prey species (Table 1). They are To test the hypothesis that there is a predator size Table 1.
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