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Metabolic Response of Antarctic Pteropods (Mollusca: Gastropoda) to Food Deprivation and Regional Productivity

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Metabolic Response of Antarctic Pteropods (Mollusca: Gastropoda) to Food Deprivation and Regional Productivity Vol. 441: 129–139, 2011 MARINE ECOLOGY PROGRESS SERIES Published November 15 doi: 10.3354/meps09358 Mar Ecol Prog Ser Metabolic response of Antarctic pteropods (Mollusca: Gastropoda) to food deprivation and regional productivity Amy E. Maas1,*, Leanne E. Elder1, Heidi M. Dierssen2, Brad A. Seibel1 1Department of Biological Sciences, University of Rhode Island, Kingston, Rhode Island 02881, USA 2Department of Marine Sciences, University of Connecticut, Groton, Connecticut 06340, USA ABSTRACT: Pteropods are an abundant group of pelagic gastropods that, although temporally and spatially patchy in the Southern Ocean, can play an important role in food webs and biochem- ical cycles. We found that the metabolic rate in Limacina helicina antarctica is depressed (~23%) at lower mean chlorophyll a (chl a) concentrations in the Ross Sea. To assess the specific impact of food deprivation on these animals, we quantified aerobic respiration and ammonia (NH3) produc- tion for 2 dominant Antarctic pteropods, L. helicina antarctica and Clione limacina antarctica. Pteropods collected from sites west of Ross Island, Antarctica were held in captivity for a period of 1 to 13 d to determine their metabolic response to laboratory-induced food deprivation. L. helicina antarctica reduced oxygen consumption by ~20% after 4 d in captivity. Ammonia excretion was not significantly affected, suggesting a greater reliance on protein as a substrate for cellular res- piration during starvation. The oxygen consumption rate of the gymnosome, C. li macina antarc- tica, was reduced by ~35% and NH3 excretion by ~55% after 4 d without prey. Our results indi- cate that there is a link between the large scale chl a concentrations of the Ross Sea and the baseline metabolic rate of pteropods which impacts these animals across multiple seasons. KEY WORDS: Pteropod · Zooplankton · Antarctica · Metabolism · Feeding · Temperature Resale or republication not permitted without written consent of the publisher INTRODUCTION regions where their populations are dense, their grazing results in a substantial flux of biogenic car- Limacina helicina antarctica (hereafter Limacina) bon from surface waters as strings of mucus-bound is a thecosomatous (shelled) pteropod that is often a discarded particles (‘pseudo-feces’, Gilmer & Harbi- major component of the planktonic community in the son 1986), remnants of mucus webs, and waste pel- Ross Sea (Hopkins 1987, Hunt et al. 2008, Ross et al. lets, sink to depth. Ac cornero et al. (2003) found that, 2008, Elliott et al. 2009). These omnivorous pelagic during certain seasons, Limacina fecal pellets were gastropods use mucus webs and ciliary action to responsible for 95.5% of the mass flux in the Ross entrain large quantities of phytoplankton, efficiently Sea. Further research suggested that pteropods ingesting ~2000 to 6000 ng of pigment ind.−1 d−1 could contribute up to 72% of the Ross Sea organic (Pakhomov et al. 2002). The unique mucus webs of carbon export during bloom periods (Manno et al. thecosome pteropods allow them to trap particles 2010). from 2 µm to ~1 mm, a size range which enables Due to their aragonite shells, thecosomatous ptero- them to feed on diatoms as well as both the unicellu- pods are also responsible for a large portion of cal- lar and colonial aggregates of Phaeocystis antarctica cium carbonate (CaCO3) flux in polar waters. These ice algae (Hopkins 1987, Gilmer & Harbison 1991). In shells have been documented to contribute substan- *Email: [email protected] © Inter-Research 2011 · www.int-res.com 130 Mar Ecol Prog Ser 441: 129–139, 2011 tially to the carbonate flux south of the Polar Front ability is linked with a rise in metabolic rate, referred (Collier et al. 2000, Honjo et al. 2000, Honjo 2004). to as the specific dynamic action (SDA). SDA is a However, the pteropod contribution to the biogeo- result of the energy required to mechanically process chemical carbon cycling in Antarctic waters is still the food and the biochemical cost of processing and not well understood, in part due to the variability in assimilating the nutrients (for review see Secor 2009). pteropod population density, lack of knowledge As a result of lower basal metabolic rates in frigid about life cycles, lack of direct measurements of dis- waters, the SDA of polar marine ectotherms often solution and sinking rates and an incomplete under- results in a lower absolute increase in oxygen con- standing of metabolic rates (Hunt et al. 2008). This sumption, but it has been shown that the effect lasts dearth of information about pteropods has become for a longer period of time (Peck & Veal 2001). The notable as the growing concerns about ocean acidifi- extended duration of SDA in these species impacts cation have highlighted the potential susceptibility of longer term patterns of production in Antarctic spe- marine calcifiers in polar regions (Seibel & Fabry cies. 2003, Orr et al. 2005, Fabry et al. 2008). There has been much speculation as to how global Aside from being prominent primary consumers of climate change will affect the already highly variable phytoplankton and important contributors to the assemblages of phytoplankton in the Southern organic carbon and CaCO3 cycles in the Ross Sea, Ocean, with uncertain implications for the carbon thecosomes are prey for seabirds, whales, fish, and budget and living biomass production (Sarmiento et crustaceans (Lalli & Gilmer 1989, Foster & Mont- al. 1998, Arrigo et al. 1999, Moline et al. 2008). Irre- gomery 1993, Hunt et al. 2008). Limacina is also the spective of whether phytoplankton mass increases or exclusive food for the gym no somatous pteropod decreases, we need a clear understanding of how Clione limacina antarctica (hereafter Clione) (Gil mer changing productivity directly impacts important pri- & Lalli 1990). All gymnosome pteropods studied to mary and secondary consumer zooplankton species. date are feeding specialists on thecosomes, consum- This study presents laboratory experiments which ing the soft bodies of their prey and discarding the compare the oxygen consumption and ammonia empty CaCO3 shells. This has led to an evolutionary excretion during the first 1 to 3 d of food deprivation arms race between the families, which links the to the next 4 to 13 d in Clione and Limacina. These behavior, morphology, and physiology of each preda- measurements inform our analysis of the metabolic tor-prey pair (Seibel et al. 2007). Very little is known rate measurements for the 2 dominant pteropod spe- about the place of Clione in the Southern Ocean food cies in the Ross Sea, Antarctica, over 5 separate sea- web. It is little reported from the guts of Antarctic sons. Our data extends previous observations made organisms, perhaps due to its novel antifeedant com- by Seibel & Dierssen (2003) to an unprecedented 5 yr pound, pteroenone, which has been shown to deter a time series that illuminates an important relationship number of fishes from feeding on it (Bryan et al. between metabolism and regional productivity. 1995). Little to no research has assessed how the biol- ogy or feeding habits of Clione might affect the bio- geochemical processes in this region. However, the METHODS particularities of its diet result in an extremely high assimilation efficiency and an unambiguous source Collection of prey (Conover & Lalli 1974), which make it a good model for investigating trophic dynamics. Ross Island is located just off the coast of the Production (growth and reproduction) in the Antarctic continent in the Ross Sea, south of New Southern Ocean is generally limited by food avail- Zealand. Here, at McMurdo Station and in the north- ability rather than temperature (Clarke 1988). Phyto- ern ice-free shorelines, we caught pteropods for our plankton levels in polar seas have been linked to in study during January and February of 2007 and 2008 situ growth rates of Antarctic krill Euphausia superba (Fig. 1). At Barne Beach, Cape Bird, Cape Royds, and both within and between seasons, with krill popula- Cape Evans, organisms were hand captured using tions responding to changing phytoplankton popula- 500 ml beakers attached to long handles, sometimes tions within a week or less (Ross et al. 2000). The referred to as ‘jelly dippers’. The pteropods were ability to respond to fluctuating food levels in a short carefully placed in plastic bottles filled with ambient period of time allows polar organisms to take advan- seawater, packed in coolers and returned to the lab- tage of the highly sporadic availability of food. The oratory at McMurdo station. There we immediately increase in growth rate during periods of food avail- transferred the pteropods into a room refrigerated to Maas et al.: Antarctic pteropod metabolic response to regional productivity 131 balance before being frozen in liquid nitrogen. Stud- ies of Limacina were conducted using the same methodology, except that individuals were incubated in 10 ml syringes because of their smaller mass. To accurately weigh these organisms, water was gently blotted from the aperture and the outside of the shell. The amount of oxygen consumed and nitrogen excreted was determined by calculating the differ- ence between control and experimental concentra- tions and incorporating the adjusted volume of water, wet mass of the organism, and time elapsed. Metabolic rate (Y) was related to wet mass (M) according to the power regression Y = aMb, where a Fig. 1. Sampling sites on Ross Island (~162° to 171° E, ~77° to 78° S). Pteropods were collected with jelly dippers from all is a normalization constant and b is the scaling coef- coastal ice-free sites and returned to the laboratory at ficient. These coefficients were then used to compare McMurdo Station the oxygen consumption rates (R) of specimens over their normothermic range (T = +2 to −2°C) resulting −2°C and moved them into 0.2 µm filtered seawater in a temperature coefficient (Q10), where Q10 = [(T2−T1)/10] in 1 l nalgene bottles.
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