Secondary Production of a Southern California Nebalia (Crustacea: Leptostraca)

MARINE ECOLOGY PROGRESS SERIES Vol. 137: 95-101, 1996 Published June 27 Mar Ecol Prog Ser

Secondary production of a Southern California Nebalia (Crustacea: Leptostraca)

Eric W. Vetter*

Scripps Institution of Oceanography, UCSD 0201,9500 Gilman Drive, La Jolla, California 92093-0201, USA

ABSTRACT: Nebalia daytoni is an abundant leptostracan crustacean from the infauna between 10 and 30 m on the sand plain off the coast of San Diego, California, USA. Secondary production of N. daytoni was estimated to be 0.930 g dry weight m-' yr.' between June 1991 and June 1992, and 0.660 g dry weight m-2 yr-' between June 1992 and June 1993. The corresponding ratios between production and biomass were, respectively, 2.92 and 3.17, less than those reported for other leptostracan species living in organically richer environments. Throughout this 2 yr study, adults accounted for most of the secondary production within the population. Few data exist for leptostracan secondary production so reports of amphipod secondary production are used for comparative purposes. Arnphipods, in general, also appear to conform to the pattern of both greater productivity in vegetated habitats, or habitats w~th large Inputs of macrophyte detntus, and the pattern of adult production.

KEYWORDS: Nebalia . Amphipod - Secondary production - Detritus

INTRODUCTION column, but do not sample the particulate carbon that enters, or passes through, patches of the seafloor hori- Increases in community production are usually zontally in the bedload and nepheloid layer. Sec- linked to increased food availability, and are reflected ondary production by benthic detritivores, which by higher biomass (Banse & Mosher 1980) or, more accounts for both the quantity and quality of the controversially, by higher production-to-bion~ass(P:B) organic matter available for higher trophic levels, is ratios of populations within the community. Because thus a crucial element in determining comm.unity com- plants are limited by light in most of the ocean, and by position and overall productivity of the benthos the unstable substratum in shallow coastal sediments, (Tenore 1988, Gage & Tyler 1991). This paper exam- most benthic and demersal food webs (and pelagic ines the secondary production of Nebalia daytoni, a webs below the photic zone) are based on plant and deposit-feeding detritivore living in a subtidal sand animal detritus rather than on viable plants (Roman plain off the coast of Southern California, USA, over a 1984, Mann 1988). The standing stock of detritus can 2 yr period. Results from this study, and published be estimated simply by determining the organic car- reports of Nebalia spp. and amphipod production, bon content of the sediment; such measures, however, were used to evaluate the hypothesis that infaunal cannot be used as indices of food available to benthic invertebrates become more productive per unit of bio- populations because much detritus is likely to be mass as the availability of organic matter increases. refractive and unavailable to detritivores (Levinton & The Leptostraca is a widely distributed, yet poorly Stewart 1988). Furthermore, such static readings give studied, order of crustaceans. Of the 7 leptostracan no insight on the rate of supply of detritus that can be genera, Nebalia is the largest, with 16 described spe- assimilated by metazoans. Sediment traps measure the cies. The habitat of N. daytoni surrounds and margin- flux of organic matter to the benthos from the water ally overlaps that of another member of the qenus. That species, Nebalia hessleri, occurs at extremely high densities within extensive mats of kelp and surf- grass detritus found in and around the La Jolla Sub-

O lnter-Research 1996 Resale of full article not permitted Mar Ecol Prog Ser 137 95-101, 1996

marine Canyon (Vetter 1995a). The secondary produc- (nearly tripllng the area sampled) Over the 2 yr of the tion of N. hessleri within the shallow reacht:s of the study 2377 individuals were sampled for production canyon was found to be among the highest reported for estimates (on average 97 9 ind mo-' in Irdr 1 and benthic macroinvertebrates (Vetter 1995b). Unlike N 100 2 ~ndmo-' in Year 2) Sedlments were llve-sleved hessleri and nearly all other members of the genus, N. with a 500 pm mesh screen withln 2 hr of collection daytoni lives in an organically impoverished environ- Samples were fixed In 4"0 formalin In sea water and ment, and is not attracted to patches enriched with stained with Rose Bengal for 48 h, after whlch they organic matter (Vetter 1996a in this issue). Because of were transferred to 70 ethanol and sorted under a the great difference in density and biomass (m-') be- dissectlng microscope to separate the N daytoni for tween the 2 species, it was obvious that annual produc- carapace measurement Measurements were made tlon (m-') of N. daytoni would be much lower than that from the anterlormost polnt (lust below the eye) to the of its local congener. Less obvious was how production posterlormost polnt of the carapace using a Wlld M5A per unit of biomass (P:B)would differ between the two, dissectlng microscope wlth ocular mlcr onleter although it was predicted that the P:B ratio of N. hess- Several non-quantitative collections were made to leri would be greater because of the abundance of food capture enough lepostracans to determine the rela- in the detritus habitat (Vetter 1995a). The P:B ratio of tlonship between carapace length and dry weight Llve N. hessleri inhabiting mats of macrophyte detritus was animals were narcotized with dilute ethanol, measured previously found to be 7.5 (Vetter 1994); the only other uslng a dissecting microscope with an ocular mlcrome- report of seconddry prodiiction for :he genus is fsr ter, c!.n.ec! to constant weight at 62' C and welqhed Nebalia sp. inhabiting seagrass meadows in Western wlth a Sartonus analytical balance Curve fits were Australia (P:B 22.5; Rainer & Unsworth 1991). carrled out using the Macintosh statistical program This study was undertaken to examine the produc- DeltaGraph Pro@ (version 3 5) tion of a numc:-ica!!y deminmt member of the lncal Secondary groductlon of Nebalia dayton~was esti- sand-plain infauna. Of more general interest, however, mated using the average-cohort method (Hynes & is the discussion of how organic enrichment affects the Coleman 1968, Hamllton 1969, Benke 1979) Thls P:B ratios of macrofaunal crustaceans. A comparison of method lnvolves calculation of the average cohort the the results from this study wlth those for other lep- average slze-frequency dlstnbutlon of the population tostracans and amphipods suggests that increased obtalned from samples taken throughout the year The availability of detritus results in greater P:B. Amphi- calculation of production involves quantifying the loss pods were chosen for comparative purposes because of biomass between successive size intervals Hamil- they have been well studied, are similar in size, and ton's (1969) modlficatlon of the basic-production equa- share many life-history characteristics with leptostra- tion of Hynes & Coleman (1968) is used here cans. The size and/or age classes of populations that are responsible for most secondary production are also P = J1- , , q x H, , (1) discussed. ]=l

where P is estimated production I is the number of tlmes the loss occurs (equivalent to the number of size MATERIALS AND METHODS classes used, the multlpllcation accounts for the limited time spent in each size class) NI 1s the mean number Field work was conducted using SCUBA from of individuals in slze class I (averaged over the entire depths of 19 to 21 m, 0.7 km off the coast of San Diego year), and I& 1s the mean dry welght of individuals be- (California, USA, 32" 52' N, 117" 15.5' W) from June longing to size class J Here PIScalculated as (1) 1,mul- 1991 to September 1994. The study area is exposed to tlplied by the product of (2) the number of animals lost oceanic swell and 1s subject to strong storm-generated in step 1 and (3) the geornetnc mean of the weight of surge during winter and early spnng Bottom water the anlmals in step I,summed for each tlme loss occurs temperature ranged from 6 to 22" C. (between slze classes) The geometric mean IS used be- Sediments were sampled monthly (from 19 to 20 m, cause it always glves a value lower than the anthmetlc as part of a larger study) using nine 7.6 cm diameter mean and more accurately reflects logarithmic growth clear butyrate tube-corers, pushed 20 cm into the sedi- patterns (Krueger & Martln 1980) The slze class inter- ment. Sampling was haphazard, with cores taken in 3 val used was 0 2 mm Instars could not be rellably den- groups of 3 cores each. Cores within each group were tlfied so were unavailable for use as a grouplng device all taken within 1 m of each other, and groups of cores This specles survived poorly In the laboratory though were separated by 4 to 8 m. Several non-quantitative 2 other specles of Nebaha that had been lababoratory samples were taken on each collection date to increase reared molted frequently wlth little change in size the number of Nebalia daytoni sampled for thls study (Nebalia sp Dahl 1985, N hesslen, Vetter unpubl ) Vetter: Secondary production of Nebalja sp. 97

Even though well over 2000 animals were collected for mum density in late spring-early summer, and mini- this study, the presumably small change in size be- mum density in late summer-early fall. tween instars made separating then1 impossible. Secondary production for the Nebalia daytoni was The secondary production calculation used here calculated for 2 yr, June 1991 through June 1993. Bio- often results in apparent gain (negative loss) of biomass was estimated using a regression equation for mass between size increments. This happens when- carapace length (CL) and dry weight (dry wt) from ever there is an increase in average abundance fresh animals [dry wt = (8.90X IO-~)X (CL)' "'l.Produc- between successively larger size groups or when there tion in the first year (Table 1) was estimated at 0.93 g is non-uniformity of growth rates between size classes. dry wt m-' ).r-'. Estimated P:B was 2.92 and average Of course negative loss is not occurring; these values density was 1087 ind. m-2 In the second year (Table 2), represent a sampling error and must be included in the the estimated P:B ratio increased to 3.17 but estimated summation to balance positive error. A curve was fltted production fell to 0.66 g dry wt m-' yr.' because of to the histogram of the average cohort, and the equa- decreased density (814 ind. m-2)and smaller average tion for that curve was used to recreate the average size (Vetter 1995a). cohort. The resulting prod.uction table did not include Averaged over 2 yr, 22% of individuals sampled any negative values and the calculated production were sexually mature (>2 mm CL; Vetter 1995a). closely matched that of the original data. Mature animals amounted to 53% of the population's The average-cohort method requires multiplying the biomass over the 2 yr study (Fig. l), and were respon- results by 365/CPI (cohort production interval = time in sible for 76"<,of production in the first year and 63 % in days from hatching to attainment of largest size class) the second year (Tables 1 & 2). to account for multiple broods (Benke 1979); however, Nebalia daytoni breed only once (Vetter 1995a), so values obtained from the calculation tables were not DISCUSSION modified. Secondary production can be estimated using published production to biomass ratios or algorithms based RESULTS on life span (in years) (Robertson 1979), adult body mass (Banse & Mosher 1980) or a combination of mean From June 1991 to June 1993, the density of Nebalia annual biomass, mean individual biomass, annual daytoni averaged 950 ind. m-2 (SD 300). with maxi- mean temperature, and depth (Tumbiolo & Downing

Table 1. Nebalia daytoni.Calculation of standing biomass and secondary production from June 199110 Ju_ne 1992 using the average cohort method (Eq.1). Size class: carapace length; N: average number of individuals of cla_ssJ; .V, - N,,,:number of individ- u:ls lost from one size class to the next; 1%: dry weight of individuals belonging to size class j; N, 14;: biomdss (dry) of size class j; W,,,: geometric mean of dry weight of 2 successive slze classes; biomass lost = NI - N,.!X E,,; P,:product~on = b~omasslost X number of times loss occurred

Size class Biomass lost p, -(mm) (4) - (9) 0.9 1.1 1.3 1.5 1.7 1.9 2.1 2.3 2.5 2.7 2.9 3.1

Density B~omass Production P B

(m-?) (a dry wt m-'! 1"$3 ,-l7,,--2 X&,+.. - ...m-2 \.:-2 '1 - - - - 1087 0.32 0.93 2.92 98 Mar Ecol Prog Ser 137: 95-101, 1996

Table 2. Nebdlia daytoni. Calculation of standing bioma? and secondary production from June 1992 to Jufe 1993 using the average cohort method (Eq. 1).Size class: carapace length; N: average number of indiv~dualsof class ,; N, - N,,,:number of indivld- uals lost from one size class to the next; W,: dry weight of individuals belonging to size_class j;_N,W,:biomass (dry) of size class j; wgm:geometric mean of dry weight of 2 successive size classes, biomass lost = y,, X Wg,; P; production = blomass lost X number of times loss occurred - Size class N NI- Q+, ? N,Lq wgm Blomass lost p) (mm) (9) (9) (g) (g) (9)

Density Biomass Production P:B (m-2) (g dry wt m") (g dry wt m-'yr-')

814 0.21 0.66 3.1.7

1994). Estimates based on such calculations may work amphipod secondary production were used for com- well in some situations, but the applicability of those parative purposes. Amphipods were chosen because of techniques is limited because of variations in growth ecological similarities between the 2 groups, and the rate as many invertebrates age (Highsmith & Coyle relatively large amount of data for amphipods. As with 1991) and increases in P:B ratios for populations of a amphipods, all species of Nebalia brood, with non- single species along a gradient of food availability planktonic juveniles exiting the brood chamber ready (Moller & Rosenberg 1982). For those reasons, and to take up the adult habitat. Amphipods and leptostra- because so little comparative data are available for lep- cans also overlap considerably in size, habitats and tostracans, production was estimated directly from trophic modes (Calman 1909, Schram 1986, Highsmlth population abundance and size frequency data. & Coyle 1991, Vetter 1995a). The effects of food supply Few data exist for leptostracan secondary production on leptostracan and amphipod secondary production (Rainer & Unsworth 1991, Vetter 1994), so reports of appear to be similar (see Table 3, and Miiller & Rosen- berg 1982). Prior to the present research, only 2 studies of leptostracan secondary production had been published. 18 Rainer & Unsworth (1991) studied a population of 16 June 1991 -June 1993 Nebalia sp, inhabiting a seagrass meadow in Western 14 m abundance Australia and reported an annual production of 5.8 y 12 a b~ornass ash-free dry wt (AFDW)m-2 and a P:B of 22.5 (Table 3). 10 n Vetter (1994) found a population of N. hessleri living 8 within subtidal accumulations of macrophyte detritus 6 with an annual production of approximately 3300 g 4 dry wt m-2 and a P:B of 7.8 (but see Vetter 1995b). Both 2 of these species occur in habitats rich in detritus and 0 both have greater secondary production and P:B ratios 0.6 1 1.4 1.8 2 2 2.6 3 3 4 3 8 than are typically reported for amphipods (Table 3). carapace length, mm The annual production for N. daytoni reported here Flg 1. Nebaliadaytonl. Abundance (hatched columns) and (0.66 to 0.93 g dry wt m-2) is lower than that of the biomass (solid columns) of animals by size. *Smallest slze other leptostracans studied because of the modest den- class with mature animals sity of N. daytoni (950 m-2)and especially its small size. Vetter: Secondary production of Nebalia sp. 99

Table 3. Reported production and P:B ratios for Nebalia and some amphipods. Where more than one report was found for an individual species, only the first found was included unless the duplicated species was included with the report of a species new to the list

Species Location Production P:B Source (g dry bvt m-' yr-')

Amphipods Ampelisca abdita New York, USA, 1-10 m 25-47 3.5-4.2 Franz & Tanacredi (1992) Pontoporeia affinis Finland, 21-25 m 7.4" 2.9 Sarvala & Uitto (1991) A. araucana Chile. 65 m 8.3 4.4 Carrasco & Arcos (1984)

A. armoricana English Channel, 17 m 10.4 2.7 Dauvin (1988d) A. ten uicornis 1.7 3.7 Dauvin (1988a) A typica 0.2 4.1-4.4 Dauvin (1988~) A. brev~cornis 0 5 2.2-2.8 Dauvin (1988b) A macrocephala Benng Sea, 35-50 m 39.8 0.9 Highsmith & Coyle (1990) A, brevicornis North Sea 0 48 3.48 Klein et al. (1975) Parhyale basrensis Iraq, ~ntertidal 5.6 3.1 All & Salman (1987) A. agasslzi Georges Bank, USA. 69-84 m 2.2 1.5 Collie (1985) Unciola inermis 2.8 2.5 Collie (1985) Ericthonius fasciatus 2.3 4.4 Collie ( 1985) Corophium volutator Sweden, intertidal 1.6-27 5.1-11.3 Moller & Rosenberg (1982) Pontopol-eia femorata Nova Scotia, Canada, 4-10 m 2.8-3.5 3.6-4.8 Wildish & Peer (1981) Gammarus mucronatus Chesapeake Bay, USA, 1 m 8 3 23.6 Fredette et al. (1990) Rhepoxynius abronius Northwestern USA, 5 m 0 6-1 1 1.3-2.1 Kemp et al. (1985) C. insidiosum Denmark, l m 0.2-8 2-5 Birklund (1977) C. volutator 2-4 3-4

Nebalia Nebalia sp Australia, l m 7 22.5 Rainer & Unsworth (1991) N. hessleri California, USA, 15-25 m 3300 7.2 Vetter (1994) N daytoni California. USA. 20 m 0.7-0.9 2.9-3.2 This study

1"Converi~on from ash free dry weight (AFDW)[dry wt = 1.25 x AFDW) I

Production per unit biomass is less sensitive to differ- supply detritus more immediately useful for growth of ences in density and size and thus is better for compar- deposit feeders (Stephenson et al. 1986). ative purposes. N. daytoni differs from the other 2 Increased productivity is usually linked to increasing members of its genus studied in possessing a consider- food availability; this is reflected by higher secondary ably lower P:B ratio (2.9 to 3.2), and living in much less production of communities and/or higher P:B ratios of organically rich conditions (Vetter 1995a). populations. Tumbiolo & Downing (1994) found that In general, vegetated habitats should support great- seagrass beds support, on average, 2.4 times the sec- er productivity than non-vegetated ones, owing pre- ondary production of other non-vegetated environ- sumably to greater food availability, habitat structure ments (for a given temperature, depth, biomass per and/or refuge from predation (Virnstein et al. 1983, unit area, and body mass). The highest P:B value for Vetter 1995a). It has been demonstrated that even amphipods in the literature was found for a population though much carbon from macrophyte detritus may of Gammarus mucronatusinhabiting a seagrass bed in remain unavailable for macrofaunal nutrition (Levin- Chesapeake Bay, USA (Fredette et al. 1990). At 23.6, ton & Stewart 1988), it still enhances the growth of its P:B value is equivalent to that of Nebalja sp, inhab- detntivores (Tenore 1975, Tenore et al. 1979, Peterson iting a similar habitat in Australia (Rainer & Unsworth et al. 1986). Vascular plants like Spartina apparently 1991; Table 3). Moller & Rosenberg (1982) estimated "eec! sn~cmicro'bia: pio~e~>i~~y'ueiore consumption the production of the amphipod Corophium volutator by macrofauna (Fenchel 1977, Findlay & Tenore 1982). at 3 locations with different grain sizes (sand, silty Thus, in comparison to vascular plants, algae should sand, and mud) and organic content (1.0, 1.6 and 3.5 %, 100 Mar Ecol Prog Ser 137.95-101, 1996

respectively).They found that both production and P:B duction/biomass relationships of f~eldpopulations. Ecol ratlos were considerably greater in populations inhab- Monogr 50:335-379 iting the more organically rich muds than at the other 2 Benke AC (1979) A modification of the Hynes method for esti- mdting secondary production with particular significance sites. Amphipods living in deeper, and supposedly less for multivoltine populations. Limnol Oceanogr 24:171-176 enriched, habitats typically have P:B ratios ranging Birklund J (1977) Biomass growth and production of the between 1.0 and 5.0 (Table 3). amphipod Corophium insidiosum Crawford and prelimi- An unexpected result was that adults produce more nary notes on Corophium volutator (Pallas). Ophelia 16:187-203 despite faster growth rates of the young. Durlng this Calrnan WT (1909) Crustacea. In: Lankester R (ed) A treatlse study, each percent of the Nebalia daytoni populat~on on zoology Adarns and Charles Black, London, p 224-243 made up by adults contributed 3.2% of the annual pro- Carrasco FD. Arcos DF (1984) Life history and production of a duction and, taken together, adults amounted to cold-temperate population of the sublittoral amphipod slightly more than half of the biomass (fig. 1). In a 2 yr Ampelisca araucana. Mar Ecol Prog Ser 14:245-252 Collie JS (1985) Life history and production of three amphi- study of a nearby population of N. hessleri inhabiting pod species on Georges Bank. Mar Ecol Prog Ser 22: subtidal mats of decaying macrophyte detritus, adults 229-238 made up 11 % of the population (numerically), 62 % of Dahl E (1985) Crustacea Leptostraca, principles of taxonomy the biomass, and 66% of the production in the first and a revision of European shelf species. Sarsia 70:135-l65 year, and 6%0 of the population, 30% of the biomass Dauvin JC (1988a) Biologie, dynamique, et production de and 43% of production in the subsequent year (Vetter populations de crustaces amphlpodes de la Manche occi- 1YY5a). For both years, each i?b of the p=pu!a::on dentale 1 Ampelisca tenuicornls Liljeborg. J Exp Mar made up by adults contributed roughly 6% of annual B101 ECOI118:55-84 production, and each percent of the population made Dauvin JC (1988b) Biologie, dynamique, et production de populations de crustaces amphipodes de la Manche occi- up by juveniles contributed roughly 0.5% of annual dentale. 2. Ampelisca brevicornis (Costa). J Exp Mar Biol pru~i~~ii~ii.Coiicen:ratisr, of bi~rr.zss anc! prndurtion Ecol 119:213-233 into the larger size classes has been frequently Dauvin JC (1988~)Biologie, dynamique, et production de reported in amphipods (Wildish & Peer 1981, High- populations de crustaces dmphipodes de la Manche occi- dentale 3. Ampelisca typica (Bate) J Exp Mar Biol Ecol smith & Coyle 1991) and, to the extent that N. daytoni 121:t-22 and N. hessleri from the detritus mat are typical, may Dauvin JC (1988d) Life cycle, dynamics, and productivity of well be the norm for leptostracans. Crustacea-Amphipoda from the western English Channel. Clearly more than 3 data points are necessary to 4. AmpeBsca armoricana Bellan-Santini et Dauvin. J Exp evaluate the relationship between food availability Mar Biol Ecol 123:235-252 Fenchel T (1977) Aspects of the decomposition of seagrasses. and growth in leptostracans; however, if one judges by In: McRoy CP, Helfferich L (eds) Seagrass ecosystems, the 3 species of Nebalia thus far investigated, lep- Vol4. Marcel Dekker, New York, p 123-145 tostracans and amphipods become more product~ve Findlay S, Tenore KR(1982) Nitrogen source for a detrit~vore: per unit of biomass as the availability of organlc mate- detritus substrate versus associated microbes. Science 218:37 1-373 rial (mostly in the form of detritus) increases. Lep- Franz DR, Tanacredi JT (1992) Secondary production of the tostracans and amphipods are also similar in that the amphipod Ampelisca abd~taand its importance in the diet adults account for most of the secondary production. of juvede winter flounder (Pleuronectes amencanus) in Jamaica Bay, New York. Estuaries 15:193-203 Fredette TJ, Diaz RJ, Van Montfrans J, 01th RJ (1990) Sec- Acknocvledgments. I am grateful to P. K. Dayton, J. T. Enright, ondary production within a seagrass bed (Zostera marina R. R. Hessler, N. D.Holland, L. A. Levin and 3 anonymous and Ruppia maritima ) in lower Chesapeake Bay. Estuar- reviewers for their critical comments on vanous versions of ies 13:431-440 this manuscript. For help with the design and fabricat~onof Gage JD, Tyler PA (1991) Deep sea b~ology,a natural history underwater equipment I thank R. R. McConnaughey. I am of organisms at the deep-sea floor. 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This article was submitted to the editor Manuscript first received: June 20, 1995 Revised version accepted: January 8, 1996