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Sieving Functional Morphology of the Gill Raker Feeding Apparatus of Atlantic Menhaden KEVIN D

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Sieving Functional Morphology of the Gill Raker Feeding Apparatus of Atlantic Menhaden KEVIN D JOURNAL OF EXPERIMENTAL ZOOLOGY 305A:974–985 (2006) Sieving Functional Morphology of the Gill Raker Feeding Apparatus of Atlantic Menhaden KEVIN D. FRIEDLAND1Ã, DEAN W. AHRENHOLZ2, JOSEPH W. SMITH2, 3 3 MAUREEN MANNING , AND JULIA RYAN 1National Marine Fisheries Service, Narragansett, Rhode Island 02882 2NOAA Fisheries Service, Pivers Island, Beaufort, North Carolina 28516 3Department of Natural Resources Conservation, University of Massachusetts, Amherst, Massachusetts 01003 ABSTRACT Menhaden occupy an important position in estuarine food webs, thus the rate processes associated with their feeding are critical to the ecosystem management of fishery and ecological resources. Atlantic menhaden feed on a wide range of plankton, the size and food quality of which change ontogenetically. We analyzed the functional morphology of the menhaden feeding apparatus in a size series of menhaden representative of juveniles and the adult migratory stock. The physical dimensions of gill arches and rakers increased isometrically with fish length; however, branchiospinule spacing, the dimension that forms the sieve apertures of the branchial basket, scaled allometrically with fish length. Juvenile menhaden from North Carolina have branchiospinule spacings that averaged 12 mm, with three arch subsections of average spacing o10 mm. Spacings did not increase with juvenile growth until the first allometric inflection point at approximately 100 mm fork length (FL). Spacing data for juveniles from other locations suggests spacing increases with latitude. Spacings increase with fish length in adults until a second inflection at 200 mm FL, after which spacing averages 37 mm. These data suggest menhaden juveniles filter smaller plankton with higher filtration efficiency than previously considered and that regional recruitment may affect adult distribution through foraging preferences. J. Exp. Zool. 305A:974–985, 2006. r 2006 Wiley-Liss, Inc. yThis article is a U.S. Government work and, as such, is in the public domain in the United States of America. How to cite this article: Friedland KD, Ahrenholz DW, Smith JW, Manning M, Ryan J. 2006. Sieving functional morphology of the gill raker feeding apparatus of Atlantic menhaden. J. Exp. Zool. 305A:974–985. The role of Atlantic menhaden, Brevoortia tyr- display similar behaviors only at larger spatial annus,inestuarineandcoastalecosystemsis scales (Kemmerer et al., ’74; Kemmerer, ’80). Thus, distinguished by their population numbers and we can estimate the distribution of various age their ability to filter extremely small plankton. menhaden among ecosystem components with a Since they are so abundant, it is assumed their filter reasonable degree of precision. However, what is feeding has a significant impact on estuarine food not clear is the fraction of the plankton community webs (McHugh, ’67). Since Atlantic menhaden are removed from the water column by the filter fished intensively, their abundance can be assessed feeding of variously sized menhaden. using virtual population analysis (Vaughan and Menhaden diet has been qualitatively described Merriner, ’91). The assessments provide age-disag- with traditional stomach content analysis gregated population sizes that can be spatially and quantitatively described by clearing rate allocated between juvenile nurseries and adult forage areas. The observed relationship between Grant sponsor: NOAA Chesapeake Bay Program Office. juvenile menhaden abundance and phytoplankton ÃCorrespondence to: Dr. K.D. Friedland, National Marine Fisheries Service, 28 Tarzwell Drive, Narragansett, RI 02882. gradients, which reflects gradient search by the fish E-mail: [email protected] (Friedland et al., ’89, ’96), suggests a predictive Received 6 July 2006; Revised 8 September 2006; Accepted 8 September 2006 capability in assessing juvenile ecosystem impacts Published online 13 October 2006 in Wiley InterScience (www. (Gottlieb, ’98; Brandt and Mason, 2003). The adults interscience.wiley.com). DOI: 10.1002/jez.a.348. r 2006 WILEY-LISS, INC. MENHADEN FUNCTIONAL MORPHOLOGY 975 experiments that estimate filtration efficiency. particles, menhaden can retain food particles The first qualitative examinations of menhaden smaller than the effective filtering efficiencies stomach contents showed that adult menhaden suggested by experiments with uniformly sized are omnivorous feeders utilizing phytoplankton cells (Friedland et al., ’84). Thus, juvenile menha- (especially diatoms and dinoflagellates), zooplank- den can graze bacteria and flagellates less than ton, amorphous matter, and material specifically 5 mm in diameter at some low rate. However, when identified as detritus (Peck, 1893). Peck hypothe- feeding at the larger end of the prey size spectrum, sized that menhaden diet composition reflected the transitional juveniles filtered some zooplank- the plankton in the surface waters they occupied. ton at a lower efficiency than phytoplankton, Subsequent stomach content work has done little suggesting the fish have maximum filtration to quantitatively test this hypothesis owing to the efficiency at a size intermediate between phyto- difficulty in accurately counting and identifying plankton and zooplankton. We are faced with menhaden food items, though new insights were the dilemma of whether it is appropriate to gained. Chipman (’59) and June and Carlson (’71) extrapolate the results of these two studies to examined the stomachs of post-metamorphic post-metamorphic juveniles (30–100 mm FL) that juveniles and observed phytoplankton and zoo- concentrate in estuarine nurseries or to young plankton in the diet, noting that juveniles con- adults (15–20 cm FL) that migrate between estu- sumed smaller zooplankton than younger larval aries along the coast. Both of these population menhaden. Jeffries (’75) used biochemical meth- segments form critical filtering components of ods to characterize zooplankton contribution their respective food webs. to the diet of juveniles. Lewis and Peters (’94) Many estuarine and oceanic processes are demonstrated the utilization of refractory cellu- governed by the production and utilization of lose by menhaden feeding near marsh habitats. plankton particles so it is easy to see where Lacking quantitative inference about menhaden incorporating menhaden into ecosystem models diet, attention turned to experimental work is essential. Estuaries face increasing threats from measuring the filtration efficiency of the fish. nutrient loading and the distribution of hypoxic An ontogenetic continuum of menhaden filter- conditions (Hagy et al., 2004). Atlantic menhaden ing ability was confirmed by two sets of clearing are among a suite of filter-feeding organisms rate experiments that characterized their ability resident in estuaries and the coastal ocean that to filter over an ecologically relevant size spectra collectively exert a controlling effect on both living of plankton. One of the clearing rate experiments and detrital particles and the nutrients and was done with a group of large migratory adults pollution they carry (Breitburg, 2002; Jung and whereas the other was done with a group of fish of Houde, 2003, 2005). The large number of menha- a transitional size between juvenile and adult. The den occurring in neritic waters represents a experiment with adults was conducted with fish significant filtering capability (Oviatt et al., ’72), averaging E260 mm fork length (FL) and showed which in addition to removing phytoplankton from that larger, older menhaden had a minimum size the water column, may also utilize detrital threshold of 13 mm diameter particles (Durbin and material to a significant degree (Lewis and Peters, Durbin, ’75). However, the clearing rate data for ’94). Menhaden feeding may accelerate the deposi- these fish also suggest that significant retention tion of material to anoxic bottom sediments (10% efficiency) does not occur for particles less through the formation of fecal pellets thus affect- than 30 mm in diameter. At the larger end of the ing the consumption of oxygen and the sequestra- prey size spectra, the adults were highly efficient tion of nutrients in the benthos (Lane et al., ’94). when filtering zooplankton. The clearing rate Since the discovery that cyanobacteria appear experiments with the transitional juvenile fish viable after gut passage through menhaden were conducted with E138 mm FL fish, which (Friedland et al., 2005), the observed shift in considering when the fish were collected, were estuarine plankton communities may in part be most likely age-1 fish that over-wintered in attributed to changes in grazing pressure on Chesapeake Bay. These fish were shown to have the plankton (Davis et al., ’97). Understanding dramatically different filtering ability from that of the grazing dynamics of the full-size range of large adults, retaining particles as small as 5–7 mm menhaden is essential to understanding the work- and showing significant retention efficiencies on ings of estuarine and coastal food webs. 7–9 mm sized particles (Friedland et al., ’84). With Relating feeding structure functional morphol- the helping effect of detritus and other plankton ogy to feeding selectively has been used effectively J. Exp. Zool. DOI 10.1002/jez.a 976 K.D. FRIEDLAND ET AL. in understanding resource partitioning in conge- for the purposes of our study fish less than 104 mm ner menhadens (Castillo-Rivera et al., ’96), among FL, were collected from estuarine locations other species, and in studying ontogenetic shifts in North Carolina, New York, Massachusetts, in feeding (MacNeill and Brandt,
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