The Relationship between Shell Morphology and Microhabitat Flow in the Endemic Hawaiian Stream Limpet (Hihiwai), Neritina granosa

The Hawaiian stream limpet, Neritina granosa Sowerby, has three shell morphologies: conic (smooth, narrow shell), intermediate (rugose, narrow shell), and winged (flattened, rugose, and flared shell margin). We studied the relationship between shell morphology and water flow in a laboratory flume and in populations from Palauhulu Stream, Maui. Winged morphs represented 82% of the population at the mouth below the terminal waterfall. At sites above the falls, conic and intermediate morphs dominated. Limpets from the mouth had significantly lower shell-length/shell-width and body-weight/shellweight ratios and occurred in areas of lower benthic and surface velocities than upstream populations. Field determinations of velocities (measured with a thermistor-based microcurrent meter) around individual N. granosa in the field that were oriented parallel to flow demonstrated that conic and intermediate morphs experienced significantly less drag than winged morphs; there was no significant effect when shells were oriented perpendicular to flow. In a laboratory flume, conic and intermediate shells oriented parallel to flow exhibited significantly greater lift and less drag than a winged morpho There was no significant difference in lift and drag for conic and winged morphs in a perpendicular orientation. Because field orientation of the three shell morphs is unpredictable, we hypothesize that microhabitat flow has little or no effect on the phenotypic expression ofshell morphology in N. granosa. We feel that the transition between winged and conic/intermediate morphs in upstream populations is restricted by bioenergetic constraints on the partitioning of energy between the competing demands of shell and tissue growth. the hydraulic regime encountered by benthic macroinvertebrates (Statzner and Holm 1982, 1989, Statzner 1988) and intertidal limpets (Denny 1989). In addition to basic body form, body ornamentations such as ribbed and/or rugose surfaces and body irregularities can potentially act as roughness elements for altering the effects of lift and drag (Vogel 1981, Denny 1989). Statzner et al. (1988) have '-rhis-projecrwadun-deu-oy,-h-e-{j~S-;-A:rmyEnng<T1.n.ne""e'"r---:e=-=m=pt:"h=-as""'I'zed the Importance of quantifying Division, Pacific Ocean. Permission was granted by the the microhabitat hydraulic regime at the Chief of Engineers to publish this information. Manuscript accepted 5 Oclober 1992. microhabitat level of benthic macroinverte2 U.S. Army Engineer Waterways Experiment Stalion, brates to more fully understand the ecologiEnvironmenlal Laboratory, Vicksburg, Mississippi 39180cal, physiological, and behavioral adaptations 6199. of these organisms to flow. 3 Department of Biology, University of Dayton, Daylon, Ohio 45469-2320. The endemic Hawaiian limpet (hfhfwai), 4U.S. Army Engineer Division, Pacific Ocean, Fort Neritina granosa Sowerby, occurs in streams Shafter, Hawaii 96858. on all of the major Hawaiian Islands. N. 264 PACIFIC SCIENCE, Volume 47, July 1993 MATERIALS AND METHODS a combination of gravel, cobble, boulder, and bedrock, and there is a dense riparian canopy of both native and introduced vegetation. Palauhulu Stream, like most Hawaiian streams, has a stair-step sequence ofwaterfall, pool, and rapids. A long-term sampling station was established in January 1990 ca. 300 m upstream of the confluence with Pi'ina'au Stream at an elevation of -40 m (= upstream site). There are three waterfalls between this upstream site and the ocean; a 6-m falls 100 m downstream of the sampling station, a 3-m falls 20 m upstream from the confluence with Pi'ina'au Stream (part of a water diversion into taro fields), and the 4-m terminal falls that empties into Waialohe Pond near the mouth of Pi'ina'au Stream. At the upstream site, water depths at median flows during 1990-1991 ranged from < 0.1 0 m in rapids to 1.5 m in pools, and water temperatures ranged from 16°C to 21°e. The hydraulic regime of Palauhulu Stream was determined on a regular basis during 1990-1991 and is extremely variable and flashy, with daily flows ranging from 0.4 to 283 m sec-l. Median flows ranged from 1.13-1.17 m sec-l. Periodic collections of limpets were also made at the Pi'ina'au mouth at Waialohe Pond (= mouth), a broad (10 m), deep (2-4 m) channel; and at the confluence of Pi'ina'au and Palauhulu streams (= confluence), a sha!low ( < I m), high-velocity riffle/run. granosa populations are generally found in shallow, well-oxygenated streams on gravel, cobble, boulder, and bedrock substrates and are restricted in distribution to streams with continuous flow (Ford 1979). This distributional restriction is believed to result from the diadromous life cycle of N. granosa in which there is an obligatory period of oceanic larval development (Maciolek 1978, Ford 1979). Vermeij (1969), Maciolek (1978), and Ford (1979) have reported the existence of two distinct shell morphologies in N. granosa: a conic morph characterized by a smooth, narrow shell and a winged morph that exhibits a flattened, crenulated shell margin and a ribbed and rugose ornamentation. Maciolek (1978) and Ford (1979) have reported a distinct gradient with respect to shell form, with the conic morph being prevalent above the first waterfalls and at higher elevations and the winged morph being found near the stream mouth. Vermeij (1969) hypothesized that the rugose shell ornamentation in this species was an adaptation to minimize the effects of drag in the high-gradient streams characteristic of Hawai'i. Ford (1979) hypothesized that shell morphology and ornamentation were attributable to environmentally induced phenotypic variation and suggested that high velocities were the principal variable affecting the growth of the mantle and an inhibition of lateral wing formation. The objectives of this study were to: (1) assess the degree of instream morphological variation in N. granosa; (2) describe the flow regime encountered by N. granosa in the field; and (3) quantify the relationship between shell morphology and orientation and flow in the field and laboratory flume. Neritina granosa is common in both Pi'ina'au and Palauhulu streams, with densities ranging from 10 to 50 m2 (e.M.W. and A.J.B., unpublished data). On 17 February St d A 1991, samples of N. granosa were collected u y rea from three sites: (1) below the terminal falls in uhulu-S~feam-is-a-thifd-0r_d~r_stl"eam____WaialoheJ~ond_(moll1h);-(2)-aLthe...-c-onfluen on the windward side of the island of Maui. ofPalauhulu and Pi'ina'au streams above the The stream originates at ca. 853 m elevation, first falls (confluence); and (3) at 40 m altitude is partially diverted at 610 m, 457 m, and 20 m and above three waterfalls (upstream). Indielevations (288 liters day-l), and is continuous viduals used for measurements of shell moruntil joining Pi'ina'au Stream above the terphology were collected by randomly selecting minal falls that empties into Waialohe Pond 0.25-m sampling quadrats in all habitat types 100 m upstream ofwhere it discharges into the (pools, runs, rapids) and removing all individPacific Ocean. The substrate in the stream is uals from substrate surfaces and the underShell Morphology and Water Flow in Neritina granoSa-WAY ET AL. 265 sides of movable rocks. Instream orientation dicular to primary velocity vectors), shell with respect to flow was noted for each limpet length, and morphological type (conic, winged, before collection. Limpets were fixed in '" 5% intermediate) of each limpet were recorded. neutral formalin in the field for subsequent Determinations of the effects ofshell shape on measurements in the laboratory. Measureambient flow regimes were approached using ments of shell length (SL = greatest anteriortwo indirect indicators of lift and drag forces. posterior dimension), shell width (SW = The relative magnitude of lift forces was greatest lateral dimension), and shell height calculated as the percentage increase in veloc(SH = greatest dorsal-ventral dimension) were ities from the leading shell edge to the shell measured to the nearest mm with hand-held apex, with steeper velocity gradients indicatdial calipers. Using Ford's (1979) criteria ing relatively greater lift forces (directed tofor conic and winged morphs, each shell ward the water surface) imparted on the shell. was categorized as morphologically conic The magnitude of drag forces was measured (smooth, narrow, rounded shell) or winged as the percentage recovery of ambient up(flattened, crenulated shell margin and a ribstream velocities I em behind the trailing shell bed and rugose ornamentation). The majority edge, with greater differences between upof limpets collected at the confluence and stream and downstream velocities indicating upstream sites had heavily ribbed and rugose greater momentum removed from the flow shells but were conic in shape. We designated and thus greater drag forces. this morphology as intermediate (between The thermistor-based current meter was conic and winged). constructed according to LaBarbera and Vogel Subsamples of 20 limpets spanning the (1976) and Vogel (1981). Sensing probes were population size range from each of the three modified for use in both high-gradient stream sites collected in February 1991 were chosen habitats and high-velocity flumes (Burky and for the determination of body-weight/shellWay 1991). Calibration of the meter and weight ratios. Conic juveniles < 20 mm SL probe was achieved with a unit that modified were excluded from this analysis. Shell length and combined designs from Vogel (1981), and width of each limpet was measured, the Muschenheim et al. (1986), and Burky and body removed from the shell, and the shell Way (1991). and tissues dried to a constant weight at Current velocities were mapped around 60°C for 24 hr. Ambient benthic and surface distinct shell morphs (conic, intermediate, and velocities were determined at the three sites. winged) of N. granosa in a 12 by 0.5 by 0.5 m Measurements were taken I em above the (length: width: height) oblong, fiberglass racesediment-water interface and I em below the track flume. Shells of N. granosa were anwater surface at 10 points spanning the width chored 20 em from the trailing edge of a 150 of the stream. by 1.5 em piece of clear Plexiglas with modeField measurements of flow velocities ler's clay and placed at one end of a 5-m around N. granosa were collected for 30 limraceway. Flows in the flume were created pets from the upstream site in July and Nousing a small, variable-speed electric boat vember 1990, and for 21 limpets from the motor anchored to the beginning of the oppomouth site in February 1991. Current velocsite raceway. The motor was capable ofgenerities were measured at points around N. graating flows up to 80 em secat the point of o:":'s~a-'u~s~i n~g~a~t"-,h~e~r~m~i~st~o ... r---;-b~a""s~e~d--,c~u,-:,-r~re"-!n~tc-'m~e-,,te~r~. ~s~h",e",ll~plac.emenLElow_chal"actef.istiGs-in-t Velocies were measured I em upstream of the flume at the experimental velocities are given shell edge, '" I mm above the shell apex, and in Table I. Current velocities were measured I em behind the downstream shell edge. Veat points around N. granosa shells using the locity measurements were also taken at 1 em thermistor-based current meter. The sensing below the water surface. Velocity measurethermistor was held in place by a stainless steel ments were based on a running average of micromanipulator that permitted x,y moveeight readings taken at IO-sec intervals. Data ments in I-mm intervals. All velocity meaon instream orientation (parallel or perpensurements were based on a running average of 266 PACIFIC SCIENCE, Volume 47, July 1993