Oecologia (1990) 82:1 11 Oecologia �9 Springer-Verlag 1990

Original papers

Gut architecture, digestive constraints and feeding ecology of deposit-feeding and carnivorous polychaetes Deborah L. Penry and Peter A. Jumars School of Oceanography WB-10, University of Washington, Seattle, WA 98195, USA

Summary. We analyze gut architectures of 42 species of marine polychaetes in terms of their anatomically distinct compartments, and quantify differences among guts in terms of ratios of body volume to gut volume, relative com- partmental volumes, total gut aspect ratios and compart- mental aspect ratios. We use multivariate techniques to clas- sify these polychaetes into 4 groups: carnivores with tubular guts; deposit feeders with tubular guts; deposit feeders with 3 gut compartments; and deposit feeders with 4 or 5 gut compartments. Tubular guts, morphological expressions of plug flow, are common among deposit feeders and may allow relatively rapid ingestion rates and short throughput times. Median gut volume per unit of body volume in de- posit feeders (31%) is twice that of carnivores (15%) and ranges up to 83% in one deep-sea species. Deep-sea deposit feeders tend to have relatively larger and longer guts than closely-related nearshore and shelf species. Guts of a number of deep-sea deposit feeders and nearshore and shelf deposit feeders from muddy environments are relatively longer and narrower as body size increases, suggesting that digestive diffusion limitations may be important. Gut vol- ume scales as (body volume)1 while ingestion rate scales as (body volume) ~ I f diet and the chemical kinetics of digestion do not change appreciably, throughput time and thus the extent of digestion of given dietary components therefore must increase as a deposit feeder grows. Digestive processing constraints may be most important in juveniles of species (especially those species with plug-flow guts) that are deposit feeders as adults.

Key words: Digestion - Gut morphology - Polychaetes Deposit feeders - Carnivores

Once food is acquired digestive processing determines an animal's rate and extent of gain of energy and nutrients. Because volume limits throughput, kinematics of digestive processing are expressed statically in gut morphologies. Thus, given an understanding of gut kinematics, compara- tive descriptions of gut morphologies can be used to infer digestive constraints and aspects of animals' feeding ecolo- gies. Optimal digestion theory (Penry and Jumars 1986, 1987) provides one basis for such inference. It postulates two basic models for digestive reaction kinetics, the Michae-

Offprint requests to: D.L. Penry

lis-Menten model for enzymatic reactions and an autocata- lytic model for microbially mediated, fermentative diges- tion. It then shows that, in general, when enzymatic diges- tion is the most important component of an animal's di- gestive strategy its gut should function as a plug-flow reac- tor. When, additionally, microbially mediated fermentation is an important component of a digestive strategy, and throughput time is not long, an animal's gut should func- tion as a mixing reactor/plug-flow reactor series (foregut fermentation) or a plug-flow reactor/mixing reactor series (hindgut fermentation). Animals using enzymatic digestion have more-or-less simple, tubular guts. In contrast the guts of animals using digestive fermentation are often character- ized by expanded chambers that allow mixing and extend mean particle residence times.

Within the framework of digestion theory we analyze gut morphologies of deposit-feeding and carnivorous poly- chaete worms from intertidal, shallow subtidal, continental shelf and bathyal environments and infer potential con- straints on digestion and foraging. We choose one major class of animals to minimize issues of between-phylum vari- ability. Since our goal is to model polychaete guts in terms of reactor components and infer general characteristics of digestive processes and foraging strategies, we describe guts in terms of anatomically-distinct, not necessarily histologi- cally-distinct or embryologically-distinct, compartments. We quantify differences in guts and gut compartments among individuals and species in basic engineering terms: ratios of body volume to gut volume and relative volumes of compartments, total gut aspect ratios (total gut length to mean diameter) and compartmental aspect ratios (com- partment length to mean diameter). Such descriptions allow us to examine scalings of body and gut parameters within and among species and to test explicit predictions about interrelationships among gut morphologies, digestive con- straints and food resources.

Predictions

Metabolic requirements generally scale as body mass or volume to the 0.7 power (Calder 1984). Ingestion rate (mass or volume time -1) for animals in general (Calder 1984) and deposit feeders in particular (Cammen 1980; Forbes and Lopez 1987) follows this pattern. If throughput time remains constant as animals increase in size, gut volume in these animals should scale as body volume to the 0.7 power. I f throughput time decreases as animals increase in size, gut volume should scale as body volume to some

power less than 0.7, and if throughput time increases as animals increase in size, gut volume should scale as body volume to some power greater than 0.7. If, within a poly- chaete species, ingestion rate scales as body volume to the 0.7 power, but gut volume scales as a function of body volume to a power different from 0.7, ontogenetic changes in digestive kinematics must occur and may indicate onto- genetic changes in diet.

Diet quality (as characterized by energetic and nutri- tional composition of food and its susceptibility to digestive reactions) decreases as body size increases in herbivorous mammals, presumably because larger animals are unable to obtain sufficient quantities of higher-quality but relative- ly rare food items (Parra 1978; Sibly 1981). Gut volume in herbivorous mammals generally scales as body mass or volume to a power of one or greater (Calder 1984), and the resulting increase in throughput time with increasing body size may be a digestive adaptation to a lower-quality diet. Self and Jumars (1988) have shown that among shal- low-water, marine polychaete species larger worms tend to be less selective for particle size, a physical parameter that, in most sediments, is inversely correlated with microbial biomass, an important food resource for deposit feeders (ZoBell 1938; Dale 1974; DeFlaun and Mayer 1983; Yama- moto and Lopez 1985). I f ontogenetic changes in diet quali- ty occur within polychaete species, we predict that changes will be in the same directions as those observed for mam- mals: diet quality should decrease as body volume in- creases, and gut volume should scale as body volume to a power greater than 0.7 - more specifically, to a power greater than or equal to 1.0. In other words, gut volume should scale at least linearly with body volume in poly- chaetes as it does in other animals. In the extreme, switches from strict carnivory or herbivory to deposit feeding would be expected as juveniles grow into adults. Analogous pat- terns of diet and body size have been observed among rep- tiles: small species of lizards tend to be insectivorous while larger species tend to be herbivorous, and hatchlings of herbivorous species tend to be insectivorous until they reach some critical body mass (Pough 1973).

Among-species patterns in gut morphology and diet quality parallel within-species patterns. Sibly (1981) pre- dicted that animals eating poorer-quality diets should have larger gut volumes than similarly sized animals eating high- er-quality food. This prediction is borne out in herbivorous birds and mammals (Sibly 1981; Hume 1982). If it holds among polychaetes, deposit-feeding species should have larger gut volumes than similarly sized carnivorous species. Among the deposit feeders, deep-sea species (species from a relatively food-poor environment) should have propor- tionally more gut volume than nearshore and shelf species (species from relatively food-rich environments). I f the pat- tern of increased relative gut volume with decreased relative diet quality is expressed anatomically in deposit-feeding polychaetes as it is in some birds (Savory and Gentle 1976; A1-Joborae 1980), deep-sea deposit feeders should have rel- atively longer guts than nearshore and shelf species - a trend that already has been observed among six species of deposit-feeding teUinid bivalves (Allen and Sanders 1966).

Diffusive limitations (of enzymes to substrates or prod- ucts to the gut wall; Penry and Jumars 1987) may be addi- tional, important digestive constraints in deposit feeders. I f digestion is limited by diffusion we expect such limita-

tions to be more important in individuals with greater gut diameters and in species ingesting relatively less permeable sediments. We predict ontogenetic changes in gut morphol- ogy with larger individuals having relatively longer, nar- rower guts; species ingesting relatively less permeable sedi- ments should be more likely to show such changes.

Methods

Species of polychaetes known to be deposit feeders or carni- vores were used in this study and were chosen to represent as many different families and, among the deposit feeders, as many different feeding guilds (Fauchald and Jumars 1979) as possible. Species were selected from three environ- ments: intertidal and shallow subtidal areas of Puget Sound, Washington; the continental shelf off Cape Hatter- as, North Carolina; and the bathyal basins of southern California (Santa Catalina Basin and San Diego Trough). Specimens from Puget Sound, Washington, were collected specifically for this study; specimens from the North Caro- lina shelf and the basins of southern California were ob- tained from archived collections of two earlier studies (Ju- mars 1974; Weston 1983, 1988). All worms were fixed in formalin and then preserved in alcohol. No relaxants were used because polychaetes continue to move material through their guts while in a relaxant bath (Jumars, pers. obs.), and thus relaxation before fixation would exchange one potential set of artifacts for another. Whole individuals were rehydrated in de-ionized water before dissection.

A total of 429 individuals of 42 species was dissected (Table 1). Gut volume, gut length and mean gut radius were calculated for each worm from a longitudinal cross- section of the gut (dorsal view) drawn using a dissecting microscope with a camera lucida. Gross anatomical features were used to distinguish regions of the gut (e.g., anterior, middle and posterior regions, gut caeca), and each region was drawn and analyzed separately (see Penry 1988 for species-by-species descriptions of gut anatomy). Our use of terms such as foregut, midgut and hindgut do not neces- sarily have embryological connotations. Pharynges of car- nivorous polychaetes were not considered to be digestive structures and were not included in gut measurements. Types, locations and numbers of gut caeca (e.g., in Arenico- lidae and Opheliidae) were noted but were not included in analyses. Body volumes of small worms (less than about 30 mm 3) were calculated from longitudinal cross-sections. Body volumes of large worms were measured by displace- ment; tentacles, large branchiae (e.g., in Terebellidae) and everted pharynges were removed before measurement. Lo- cations and volumes of sediment in guts were recorded, and sediment composition was described qualitatively (i.e., sand, muddy sand, sandy mud, mud).

The longitudinal, cross-sectional outlines of bodies and guts were digitized using a video system (Motion Analysis Corporation, Santa Rosa, California) and described as a series of x and y coordinates of pixels. Given the assump- tion that each worm was cylindrical in transverse cross sec- tion, a radius, ri, was calculated at each point, xi, along the axis of the longitudinal cross section (i= 1 to n, where n is the total number of pixels along the axis of the longitu- dinal cross-section and represents the number of transverse cross-sections into which any given longitudinal outline can be divided). The volume, vl, of each transverse cross section

Table 1. List of species and collection locations (n=number of specimens analyzed). CA=California; NC=Nor th Carolina; W A x Washington

Species n Collection location Species n Collection location

Ampharetidae

Amphicteis scaphobranchiata 16 Puget Sound, WA Ampharete acutifrons 10 Cape Hatteras, NC Ampharete americana 10 Cape Hatteras, NC Anobothrus sp. A 9 San Diego Trough, CA Ecamphicteis elongata 6 San Diego Trough, CA

Arenicolidae

Abarenicola pacifica 23 Puget Sound, WA A. vagabunda 14 Puget Sound, WA

Capitellidae

Capitella cf. eapitata 10 Puget Sound, WA

Cirratulidae

Cirratulus cirratus 10 Puget Sound, WA Tharyx multifilis l0 Puget Sound, WA T. lutieastellus 9 San Diego Trough, CA Chaetozone cf. setosa 11 Santa Catalina

Basin, CA

Fauveliopsidae

Fauveliopsis glabra 10 San Diego Trough, CA

Glyceridae

Glycera americana 7 Cape Hatteras, NC G. dibranchiata 4 Cape Hatteras, NC

Hesionidae

Ophiodromus pugettensis 10 Puget Sound, WA

Maldanidae

Euclymene reticulata 20 Santa Catalina Basin, CA

Nephtyidae

Nephtys caeca 2 Puget Sound, WA N. caeeoides 16 Puget Sound, WA N. picta 10 Cape Hatteras, NC Aglaophamus paucilamellata 6 San Diego Trough, CA

Nereidae

Ceratocephale pacifica 10 San Diego Trough, CA

Opheliidae

Armandia agilis 9 Cape Hatteras, NC A. maculata 10 Cape Hatteras, NC Ophelina acuminata 6 Puget Sound, WA Travisiafoetida 12 Abyssal plain off

Baja, CA

Paraonidae

Levinsenia oculata 10 Santa Catalina Basin, CA

Polynoidae

Harmothoe extenuata 10 Cape Hatteras, NC

Scalibregmatidae

Scalibregma inflatum 23 Puget Sound, WA S. inflatum 10 Cape Hatteras, NC

Spionidae

Pseudopolydora kempijaponica 10 Puget Sound, WA Paraprionospio pinnata 10 Cape Hatteras, NC Spiophanes cf. bombyx 10 San Diego Trough, CA

Sternaspidae

Sternaspisfossor 6 Santa Catalina Basin, CA

S. scutata 13 Puget Sound, WA

Terebellidae

Artacamella hancocki 8 San Diego Trough, CA Eupolymnia heterobranchia 12 Puget Sound, WA Neoamphitrite robusta 6 Puget Sound, WA Polycirrus eximius 10 Cape Hatteras, NC Thelepus crispus 9 Puget Sound, WA

Trichobranchidae

Terebellides stroemi 12 Cape Hatteras, NC Terebellides ef. stroemi 10 San Diego Trough, CA

was est imated as the volume of a cylinder of radius, rl (pix- els), and height of one pixel; total volume was calculated as the sum o f all volumes, v~, for i = 1 to n. Measurements in pixels were converted to millimeters using digitized refer- ence scales.

The two assumptions central to the video method for determining volumes are that the body or gut axis is paral lel to the x axis of the video-digitizing system and that the body or gut is circular in transverse cross section. The sensi- tivity of results to violations of these assumptions was tested by compar ing volumes measured by displacement with vol- umes calculated from digitized longitudinal outlines (Penry 1988). Deviat ions of the body or gut axis from orientat ions parallel to the video axis were found to be a lesser source of error in the volume estimates than were deviations from the assumption that the body or gut is circular in transverse cross section. This second source of error was most impor- tant in computa t ions o f body volume and was mit igated by assuming an elliptical transverse cross section for species

that were obviously not circular. Major and minor axes of an elliptical cross section were defined, respectively, by the mean radii of a dorsal, longitudinal cross section and a lateral, longi tudinal cross section.

Classification (Wishart 1975) and discriminant analysis (Nie et al. 1975) were used to identify and analyze group- ings of individuals based on body and gut descriptors. Two divergent classification methods were used in parallel in an a t tempt to eliminate analytical artifacts. The dissimilar- ity measure in the first (" Eucl idean" method) was squared Euclidean distance with Ward ' s method of sorting. The dis- similarity measure in the second (" Canbe r r a " method) was the Canberra metric coefficient with the average-linkage method of sorting. To identify between-group differences, direct discriminant analysis was used when the number of variables was small (m = 4). Stepwise discriminant analysis (minimization of Wilks lambda) was used when the number o f variables was large (m = 16) to identify more easily the subset of variables with discriminating power.

Results

Analyses o f a priori species groups

Two groups, deposit feeders (n= 354) and carnivores (n = 75), were identified a priori (i.e., before analysis as part of the study design) and were analyzed using direct discrimi- nation. Each individual was treated as a separate case de- scribed by four measures, body volume (B), gut volume (G), gut length (L) and mean gut radius (R). Since body volumes and gut volumes ranged over five orders of magni- tude, natural log transformations of B and G were used in all multivariate analyses. The ratio B/G, body volume to gut volume, distinguishes deposit feeders from carni- vores: median B/G for deposit feeders is 3 (.95% C.L. of the median = 3 to 4; range = 1 to 10); median B/G for carni- vores is 7.5 (95% C.L. of the median=5 to 11; range=4 to 21).

Among the deposit feeders some of the intraspecific variation in B/G can be attributed to variations in gut full- ness (volume of sediment in the gut). In 6 of the 11 species exhibiting the greatest intraspecific variations in B/G (i.e., B/G range > 4) there is a significant trend in increasing B/G with decreasing percent gut fullness calculated as the ratio of measured sediment volume to measured gut volume (Kendall's r; ~=0.05 for each test); the combination of probabilities for all 11 tests is also significant (P=0.001, Fisher's method for combining independent probabilities, Fisher 1970).

Deposit feeders can be assigned to groups based on any number of single criteria or combinations of criteria: for example, they can be grouped by functional guilds (e.g., surface or subsurface deposit feeders, motile or sedentary species), by characteristics of sediment in their guts (sand, muddy sand, sandy mud, mud), or by environments (e.g., nearshore, shelf, deep sea). Two groups of deposit feeders, surface (n = 204) and subsurface (n = 150), were examined using discriminant analysis (direct method: variables= ln(B), ln(G), L, R) and could not be distinguished reliably using these general body and gut parameters. Since it was not obvious, a priori, if or how these two groups should be subdivided further, classification analyses were used a posteriori to identify species groups for subsequent discrim- inant analyses.

A posteriori identification and analysis o f species groups

In these analyses each species, described by median values of gut parameters, was treated as a separate case (n=41; Nephtys caeca and N. caecoides were combined as Nephtys spp.) to avoid weighting species in proportion to the number of individuals dissected. The set of variables was expanded to include ratios of body volume to gut volume (B/G) and total gut aspect ratio (TAR), gut compartment aspect ratios, and gut compartment volumes expressed as percentages of total gut volume. These standardized vari- ables were used because initial results showed that species tended to cluster on the basis of absolute body and gut volumes. As few as one and as many as 5 anatomically- distinct gut compartments were identified in the species ex- amined (Table 2). A matrix of 41 species by 16 gut parame- ters was generated in which each species was described by the overall gut parameters B/G and TAR and some subset of the remaining 14 gut compartment parameters.

We then identified the species that clustered together

Table 2. Anatomical definitions of the gut compartments used to classify species

Definition Key to Figure 1

I. Species with one gut compartment

Fore- and midgut not anatomically distinct from hindgut. Entire gut was coded as "hindgut" (H) in classification analyses.

II. Species with two gut compartments

Anatomically-distinct foregut (F) and hindgut (H).

III. Species with three gut compartments Anatomically-distinct fore- (F), mid- (M), and hindgut (H).

H ES

F H

F M H

IV. Species with four or five gut compartments

A. Midgut subdivided into two ana- tomically-distinct subregions: a nomnuscular, anterior subre- F A['~ ~I H gion (AM)and a nonmuscular, I ! ! N / ~ E ~ i i i [ posterior subregion analogous to [.~t.ij ....... A::::::i:: the single midgut compartment (M) defined in III above.

B. Midgut subdivided into two ana- tomically-distinct subregions: F A ] ~ DM H a nonmuscular, anterior subre- gion (AM) and a muscular, posterior subregion (PM).

C. Midgut and hindgut each subdi- vided into two anatomically-dis- tinct subregions: F AM PM AH PH Midgut: anterior subregion (AM) ~,..~ , and posterior, muscular subregion (PM). Hindgut: anterior subre- gion (AH) and posterior subre- gion (PH).

consistently in both classification analyses (Table 3). A sub- set of 26 species falling into 4 groups was thus selected and examined using stepwise discriminant analysis. The bio- logical interpretation of these results is quite clear: these 26 species are grouped on the basis of general feeding strate- gy (carnivores vs deposit feeders as distinguished by B/G) and gut architecture (numbers and types of gut compart- ments identified using gross anatomical characteristics). The four groups are (Fig. 1): (1) carnivores; (2) deposit feeders with more or less simple, tubular guts, i.e. species with only 1 or 2 anatomically-distinct gut compartments; (3) deposit feeders with 3 gut compartments, i.e. species with anatomically-distinct fore-, mid-, and hindguts; and (3) deposit feeders with 4 or 5 gut compartments, i.e. species in which the midgut and/or hindgut can be further subdi- vided into anatomically-distinct subregions.

We changed the groups assignments of 3 of the 26 spe- cies when the results of discriminant analysis suggested that they were misclassified initially. Abarenicola pacifica was reassigned to group 3 ; Armandia agilis and Fauveliopsis gla- bra were both reassigned to group 2. We then assigned the remaining 15 species to the four groups on the basis of affinities in the classification analyses that were used to select the initial subset of 26 species (Table 3). These

Table 3. Four groups of species defined on the basis of similarities in feeding strategies and gut architectures, and the results of within-species regressions of gut volume, G (mm3), versus body volume, B (mm3), and mean gut diameter, D (mm), versus gut length, L (ram). The 26 species that clustered together in both classification analyses and the groups to which they were assigned initially are indicated by the numbers in parentheses (see text for explanations of subsequent reassignments). PS = Puget Sound, NC = Nor th Carolina, and S D T = San Diego Trough, Sediment in the gut was described qualitatively: S = sand; MS = m u d d y sand; SM =sandy mud; M = m u d . B/G is the median ratio of body volume to gut volume, and TAR is the median ratio of gut length to gut diameter. Median gut volumes are given in Fig. 1. Regressions were performed using natural log transformations of the variables. See Table 1 for the number of individuals in each sample. The regression coefficient is m with its s tandard error (SE), and the regression constant is In (b) with its standard error (SE). The F ratio, with associated probability, P, was used to test the significance of each regression (Ho : m = 0; Ha :m + 0). Probabilities : * = 0.01 < P < 0.05; ** = 0.001 < P _< 0.01 ; *** = P _< 0.001

Species Sedi- B/G TAR Body Volume (ram 3) ment in gut

Regression of ln(G) vs In (B): In(G) = m[ln(B)] + ln(b)

Regression of In (D) vs In(L): ln(D) = m[ln(L)] + ln(b)

Median Range P m (SE) ln(b) (SE) P m (SE) In(b) (SE)

G R O U P 1 : Carnivores

Nephtys spp. (1) - 11.7 84 800 450-21000 *** Glyeera dibranchiata (1) - 6.5 82 65 10-170 * Glyeera americana - 9.8 99 100 40-200 ** Ophiodromus - 6.5 16 42 25 92 ***

pugettensis (2) Nephtyspieta (1) - 6.6 85 12 4-50 *** Harmothoe extenuata - 12.9 21 2 0.3-10 *** Ceratocephale - 4.7 57 3 0.2-9 ***

pacifica (2) Aglaophamus 6.4 15 0.3 0.2-2 ***

paucilamellata (2)

G R O U P 2: Deposit feeders with simple, tubular guts

Capitella cf. M 5.5 48 20 2-300 *** capitata (2)

Euclymene reticulata M 3.8 76 7 2-40 *** Armandia agilis (3) S 2.7 36 11 0.1-40 *** Armandia maculata (2) S 2.9 26 2 0.1-30 *** Tharyx multifilis (2) M 2.5 32 14 4-25 *** Paraprionospio M 4.3 87 14 8-20 *

pinnata Cirratulus cirratus M 1.9 18 2 1-14 *** Pseudopolydora S 2.4 29 4 2-8 **

kempi japonica (2) Tharyx luticastellus M 1.2 40 5 3-8 *** Chaetozone cf. setosa M 4.0 65 2 0.1-3 *** Fauveliopsis glabra (3) M 5.1 23 0.1 0.1-3 *** Spiophanes cf. bombyx M 4.0 31 0.2 0.2-2 *** Levinsenia oculata (2) M 2.4 83 0.6 0.3-1 ***

G R O U P 3 : Deposit feeders with three anatomically-distinct gut compartments

Abarenicola S 2.8 43 200 10-1550 *** pacifica (2)

Sternaspis scutata M 2.7 72 110 15-280 *** Amphicteis M 3.8 30 85 10-250 ***

scaphobranchiata (3) Ophelina acuminata M 3.2 37 65 50-170 * Artacamella M 2.0 30 4 1-100 ***

hancocki (3) Scalibregma inflatum M 1.9 19 30 20-70 ***

(from PS) (3) Ampharete M 3.9 24 18 0.4-40 ***

acutifrons (3) Ampharete M 4.3 24 2 1-20 ***

americana (3) Scalibregma inflatum S 4.4 26 5 2-16 ***

(from NC) (3) Sternaspisfossor (2) M 3.8 142 6 4-12 * Ecamphieteis M 3.2 45 4 1-6 **

elongata (3) Anobothrus sp. A (3) M 3.6 24 0.4 0.1-1 ***

1.1 (0.10) --3.0 (0.70) *** 0.9 (0.12) --3.9 (0.52) 0.9 (0.12) --1.8 (0.47) 0.14 1.7 (0.71) --7.0 (2.6) 1.1 (0.20) --2.5 (0.92) 0.17 0.7 (0.44) --3.3 (1.7) 1.2 (0.18) - 2 . 8 (0.69) *** 0.5 (0.10) - 1 . 6 (0.25)

0.8 (0.12) - 1 . 6 (0.34) ** 0.4 (0.10) --2.5 (0.32) 1.0 (0.06) --2.8 (0.08) *** 0.8 (0.05) --2.8 (0.08) 1.0 (0.05) - 1 . 6 (0.07) *** 0.6 (0.04) --3.1 (0.10)

1.1 (0.08) --1.8 (0.10) * 0.8 (0.21) - 2 . 4 (0.19)

1.1 (0.05) --1.7 (0.18) * 0.5 (0.20) - 2 . 2 (0.66)

1.2 (0.07) - 1 . 6 (0.14) *** 0.8 (0.07) --3.7 (0.23) 1.1 (0.03) --1.4 (0.09) *** 1.0 (0.06) - 3 . 5 (0.16) 1.1 (0.07) - 1.4 (0.13) *** 1.0 (0.09) --3.4 (0.19) 1.0 (0.07) --0.8 (0.19) 0.52 0.2 (0.29) - 1 . 0 (0.86) 0.9 (0.35) - 1 . 1 (0.92) 0.06 0.5 (0.23) --2.7 (0.80)

1.1 (0.10) --1.3 (0.13) * 0.4(0.18) --1.9 (0.36) 1.0 (0.26) - 0 . 8 (0.39) 0.33 0.2 (0.18) 1.3 (0.42)

1 . 0 ( 0 . 1 3 ) - - 0 . 5 ( 0 . 2 3 ) 0.33 0 . 2 ( 0 . 2 0 ) - 1 . 4 ( 0 . 5 8 ) 0.8 (0.06) --1.4 (0.06) *** 0.6 (0.12) --3.2 (0.30) 1.0 (0.05) - 1 . 4 (0.09) ** 0.5 (0.12) - 2 . 3 (0.16) 0.7 (0.12) - 1 . 9 (0.16) * 0.4 (0.14) - 2 . 7 (0.22) 1.0 (0.14) --0.9 (0.08) 0.52 0.1 (0.19) --2.2 (0.51)

0.9 (0.05) - 0 . 7 (0.25) *** 1.0 (0.06) --3.4 (0.25)

1.0 (0.04) -- 1.2 (0.20) *** 0.5 (0.06) --2.4 (0.26) 1.0 (0.06) - 1 . 3 (0.29) *** 0.8 (0.09) --2.7 (0.33)

1.0 (0,26) - 1 . 5 (1.1) * 0.8 (0.22) --2.9 (0.75) 1.0 (0.08) --1.1 (0.19) *** 0.8 (0.08) --3.0 (0.22)

1.0 (0.09) --0.7 (0.30) ** 0.5 (0.15) - 1 . 4 (0.44)

1.0 (0.05) --1.5 (0.14) *** 0.9 (0.07) --2.7 (0.18)

0,9 (0.04) - 1 . 5 (0.05) *** 0.8 (0.16) --2.9 (0.33)

1.2 (0.19) --1.9 (0.30) 0.06 0.6 (0.25) --2.4 (0.59)

0.7 (0.23) --0.8 (0.46) * 0.6 (0.14) --3.4 (0.49) 0.8 (0.13) --0.9 (0.17) 0.08 0.5 (0.23) - 2 . 5 (0.60)

0.9 (0.06) --1.3 (0.09) ** 0.3 (0.07) --2.3 (0.11)

6

Table 3 (continued)

Species Sedi- ment in gut

B/G TAR Body Volume (ram 3) Regression of In(G) vs In(B): In(G) = m[ln(B)] + In(b)

Median Range P m (SE) In(b) (SE)

Regression of In (D) vs In(L): In (D) = m [ln(L)] + In (b)

P m (SE) In (b) (SE)

GROUP 4: Deposit feeders with

Neoamphitrite M robusta (4)

Abarenicola vagabunda S Thelepus crispus SM Travisia foetida M Eupolymnia S

heterobranchia (4) Terebellides cf.

stroemi (SDT) (4) Polycirrus eximius Terebellides stroemi

(from NC)

four or five anatomically-distinct gut compartments

4.4 65 22000 15000-24000 * 0.6 (0.23) 2.2 (2.3)

3.1 35 5000 2000-20000 *** 1.0 (0.06) --1.4 (0.53) 3.9 40 4900 3500-5600 ** 0.9 (0.27) --0.9 (2.3) 2.4 23 870 4-4000 *** 1.0 (0.02) --1.3 (0.15) 3.3 28 780 400-2200 *** 1.0 (0.10) --1.3 (0.68)

M 2.8 44 2 0.3-70 *** 1.1 (0.07) -1.2 (0.15)

MS 3.0 32 7 1-38 *** t.0 (0.05) -- 1.0 (0.12) MS 3.7 31 3 1-12 *** 0.9 (0.04) --1.2 (0.06)

0.99 0.0t (0.46) 1.5 (2.6)

*** 1.0 (0.09) - 3 . 2 (0.42) 0.94 -0 .04 (0.45) 1.4 (2.2) *** 0.9 (0.11) - 2 . 7 (0.44)

** 0.6 (0.14) - 1 . 7 (0.58)

*** 0.8 (0.14) --3.3 (0.38)

*** 1.i (0.16) --4.0 (0.44) *** 0.8(0.15) --2.8(0.33)

Carnivores Glycera spp.

Ophiodromus pugettensis

Harmothoe extenuata

Nephtys spp.

Neph tys p ic ta

Aglaophamus paucilamellata

Ceratocephale pacif ica

Deposit feeders wi th Armandla maculata

Armandia agil is

Cirratulus cirratus

Tharyx mu l t i f i l i s

Tharyx luticastel lus

Chaetozone cf. setosa

Fauvellopsls glabra

Capitella cf. capitata

Pseudopo lydora kempl japonica

Parapr ionosp iop Irma ta

Spiophanes cf, bombyx

Euclymene retlculata

Levinsenia oculata

( I 0 ) I

(6) I

(0.2) [

(69)

(2)

(0,05)

(0.7)

m i

Deposit feeders wi th 3 gut compartments

simple, tubular guts (0.8) .... ~*~ i

(4 ) ............. I

( 0 , 6 ) I I

(6) =l ]

(4 ) " '--~"~

(0,4)

i Abarenicola pacif ica

I Ophelina acuminata

) Scalibregma inflatum (PS)

i Scalibregma inflatum (NC)

Sternaspis scutata

Sternaspis (2 ) .............. um: , : , :~ fossor

Amphicteis scaphobranchiata ( 22 )

Ampharete acutifrons (4 )

Amphare te americana (0,4)

Anobothrus sp. A (0 .1 )

Ecamphicteis elongata (1 )

Artacamella hancocki (2 )

( 70 ) = i : : : : : : : l J

( 16 ) ~ i

( 1 ) ~ ! ; ! ; ~ ; ! : ! ; ! ; : i I

~ : F ~ ; : : : : l J

= : : : : : : : : : 1 I

Deposit feeders wi th 4 or_5 g.~! compartments

Travisia foetida ( 3 6 0 ) ~ I H I ( 0 . 06 ) ............... ~ I

A b a r e n i c o l a vagabunda ( 1 5 5 0 ) ~==~FfA',!:~:~:l I (4)

Polycirrus eximius (2) = ~ ' / / . ~ ,

( 2 ) i i Thelepus crlspus ( 1 2 2 0 ) ~

b (3) ~ I Eupolymnia heterobranchia ( 2 3 0 ) ~ . . . . . . .

b (0 .06 ) .............. ~ J Neoamphltrlte robusta ( 5 0 0 0 ) ~ . . . . . . . . . . . . . . . . . . . .

(2 ) . . . . . . . . . . . . . . . . . . I Terebellides stroemi (NC) (0 .7 ) ~ f

(0 .3 ) t ~ Terebellidescf. stroemi(SDT)(0.8) ~ . . . . . . . . .

Fig. 1. Gut schematic showing anatomical compartmentalization. To facilitate visual comparisons of relative gut and compartmental lengths and diameters these gut schematics are normalized to gut volumes. Median gut volumes (mm 3) are given in parentheses to provide absolute size references. Relative diameters are exaggerated by a factor of 2, i.e. the ratio of the vertical (gut diameter) scale to the horizontal (gut length) scale is 2:1. See Table 2 for definitions of gut compartments and a key to symbols. Glycera spp.=G, dibranchiata and G. americana; Nephtys spp.=N, caecoides and N. caeca, m=thick-walled, muscular region immediately posterior to the pharyngeal sheath in Glycera spp. b = muscular bulb seen in 2 of the 3 spionids examined. PS = Puget Sound, Washington; NC = North Carolina; SDT = San Diego Trough, California

f inal 4 groups ( n = 4 1 species) were examined us ing stepwise d i sc r iminan t analysis (Table 4).

F o r 4 species the f inal g roup ass ignments de te rmined us ing classif ication differed f rom the g roup ass ignments tha t we wou ld have predic ted based on our knowledge of their feeding strategies an d gut morphologies . T h e carni-

vores, Aglaophamus paucilamellata, Ceratocephale pacifiea, a n d Ophiodromus pugettensis, were assigned to group 2 when we wou ld have predicted that they would be assigned to g roup 1, and the deposi t feeder, Sternaspis fossor, was assigned to group 2 when we wou ld have predicted it would be assigned to group 3. We thus r an the d i sc r iminan t analy-

Table 4. Results of the discriminant analysis of 41 species assigned to four groups: carnivores (group 1), deposit feeders with tubular guts (group 2), deposit feeders with three gut compartments (group 3), and deposit feeders with four or five gut compartments (group 4). See Table 2 for definitions of gut compartments and Table 3 for the species in each group. The discriminant functions classify correctly 100% of the species

Discriminant function

I tI III

A. Discriminating power of the variables

Wilks lambda 0.0008 Chi-square probability ~ 0.0001

0.020 0.241 40.0001 40.0001

B. Discriminant functions

Eigenvalue 25 12 2.8 Discriminating variables and coefficients

Ratio of body volume -0.29 --0.07 0.87 to gut volume

Total gut aspect ratio (TAR) 0.26 --0.45 0.25 Aspect ratio of foregut (F) 0.13 0.42 -0.62 Aspect ratio of anterior 0.85 1.32 0.24

subregion of midgut (AM) Aspect ratio of posterior -- 0.2t 0.70 -- 0.30

subregion of midgut (PM) Volume of foregut (F) 0.04 -0.68 -0.34 Volume of midgut (M) 1.32 0.12 0.22 Volume of anterior -0.58 0.47 0.02

subregion of midgut (AM) Volume of posterior 0.85 1.23 0.40

subregion of midgut (PM) Volume of posterior 0.44 0.43 0.35

subregion of hindgut (PH)

C. Group means

Discriminating variables Ratio of body volume 8.1 3.3 3.3 3.3

to gut volume Total gut aspect ratio (TAR) 57.4 45.7 43.0 37.2 Aspect ratio of foregut (F) 0 9.0 6.8 7.8 Aspect ratio of anterior 0 0 0 0.6

subregion of midgut (AM) Aspect ratio of posterior 0 0.3 * 0 2.8

subregion of midgut (PM) Volume of foregut (F) 0 8.2 7.6 4.5 Volume of midgut (M) 0 0 61.2 16.8 Volume of anterior 0 0 0 2.5

subregion of midgut (AM) Volume of posterior 0 1.0 * 0 12.0

subregion of midgut (PM) Volume of posterior 0 0 0 9.5

subregion of hindgut (PH)

* The presence of small, muscular gut bulbs in 2 spionids, Para- prionospio pinnata and Spiophanes cf. bombyx (see Fig. 1), results in these non-zero values

sis twice, once using the classification assignments for these 4 species and once using our predicted assignments. The results were essentially identical. One additional discrimi- nating variable, the volume of the anterior subregion of the midgut identified in worms in group 4 (see Table 2), was identified when the predicted assignments were used, but in both analyses all 41 species were classified correctly

Table 5. Comparisons of ratios of body volume to gut volume (B/G) and median standard gut lengths (SL): deep-sea species ver- sus nearshore and shelf species Ho: B/G's of deep-sea species >__ B/G's of nearshore and shelf spe-

cies. H,: B/G's of deep-sea species < B/G's of nearshore and shelf spe-

cies. Ho: SL's of deep-sea species_< SL's of nearshore and shelf species. Ha: SL's of deep-sea species > SL's of nearshore and shelf species.

Species B/G Pairwise SL Pairwise com- com- parisons parisons

Deposit feeders with tubular guts

Cirratulidae

Deep sea Tharyx luticastellus 1.2 64 +, + Chaetozone cf. setosa 4.0 + i + 84 +, +

Nearshore Tharyx multifilis 2.5 49 Cirratulus cirratus 1.9 45

Spionidae

Deep sea

Spiophanes cf. bombyx 4.0 + , - 58 + , - Nearshore and shelf

Pseudopolydora 2.4 45 kempi japonica

Paraprionospio pinnata 4.3 97

Deposit feeders with three gut compartments

Ampharetidae and Terebellidae

Deep sea Anobothrus sp. A 3.6 , , 49 - , + , + Ecamphicteis elongata 3.2 , , 65 +, +, + Artacamella hancocki 2.0 , , 54 + , + , +

Nearshore and shelf Amphicteis 3.8 51

seaphobranehiata Ampharete aeutifrons 3.9 39 Ampharete americana 4.3 46

Sternaspidae

Deep sea Sternaspisfossor 3.8 + 149 +

Nearshore

Sternaspis seutata 2.7 91

Deposit feeders with four or five gut compartments

Terebellidae and Trichobranchidae

Deep sea Terebellides cf. stroemi 2.8 . . . . 58 +, - , - , +, +

Nearshore and shelf Eupolymnia heterobranehia 3.3 51 Neoamphitrite robusta 4.4 85 Thelepus crispus 3.9 61 Polycirrus eximius 3.0 55 Terebellides stroemi (NC) 3.7 31

Binomial Test 17(+), 4 ( - ) P = 0.025

17(--), 4 (+) P = 0.025

by the discriminant functions. Since they make more sense to us biologically, we have chosen to present in Table 4 the results obtained when our predicted assignments for these four species are used.

Interspecific patterns in body and gut parameters

We expected that deep-sea deposit feeders would have pro- portionally larger guts and relatively longer guts (i.e., smaller B/G's and greater standard gut lengths, a relative measure of gut length scaled to a constant body volume to eliminate differences in body size) than nearshore or shelf deposit feeders. Tests of this hypothesis must be limited to comparisons of closely-related taxa within groups de- fined on the basis of similarities in gut architecture. Com- parisons thus are possible among the cirratulids, spionids, sternaspids, the ampharetids and terebellids in group 3, and the terebellids and trichobranchids in group 4, but not, for example, among the opheliids because the 4 species fall into three different gut-architecture groups. Median values of B/G and standard gut length were used for each species (Table 5). These comparisons suggest that the deep-sea spe- cies do tend to have proportionally larger guts and relative- ly longer guts than nearshore or shelf species.

Intraspecific patterns in body and gut parameters

Morphometric relationships between body volume and gut volume and between mean gut diameter and total gut length were examined for each species using parametric regression with natural log transformations of the variables (Nie et al. 1975). Body volume and gut length were chosen as the independent variables since they could be estimated with less error than gut volume and mean gut diameter. Regres- sions of the natural log of gut volume versus the natural log of body volume (ln G = m (ln B)+ln(b), where m is the regression coefficient, and ln(b) is the regression con- stant) are significant in all cases: Gut volume can be ex- pressed as some positive power of body volume, G = b B m, (overall F's for regressions: P < 0.05) (Table 3). Gut volume scales as body volume to some power greater than 0.7 and not significantly different from 1.0 in 21 of 33 deposit feed- ers and 5 of 8 carnivores (95% C.L.'s on regression coeffi- cients do not include 0.7 but do include 1.0). In the remain- ing species the 95% confidence limits on the regression coef- ficients include both 0.7 and 1.0, but in 4 of these species, all deposit feeders, 0.7 is the lower limit. Unlike the results of comparisons of herbivorous and carnivorous mammals (Calder 1984) there appears to be no difference in the scal- ing of gut volume with body volume between deposit-feed- ing and carnivorous polychaetes. The relatively small number of carnivorous species analyzed (8 spp.) and the relatively small numbers of individuals examined within each carnivorous species (about 10 individuals per species), however, limit our ability to detect differences in scaling if they exist.

Regressions of the natural log of mean gut diameter versus the natural log of gut length (ln D =m( ln L)+ln(b) are significant in 33 species: Mean gut diameter can be expressed as some positive power of gut length, D = b L TM

(overall F's for regressions: P_< 0.05) (Table 3). The regres- sion coefficient, m, is less than 1.0 in 17 of these 33 species (Ho :m_> 1.0, and H, :m < 1.0; one-tailed t-test, ~= 0.05) in- dicating that total gut aspect ratio tends to increase as gut length increases in each of the 17 species. These 17 species include 4 of 8 carnivores, 7 of 12 deep-sea deposit feeders and 6 nearshore and shelf deposit feeders from muddy envi- ronments.

Discussion

Gut architecture and diet quality

All carnivorous polychaetes examined have very simple guts while deposit feeders may have more elaborate, compart- mentalized guts. As we predicted, carnivorous polychaetes have significantly less gut volume per unit of body volume than do deposit-feeding polychaetes, a difference that can be attributed directly to diet quality. Diets of carnivorous polychaetes obviously contain greater proportions of high- quality foods (i.e., higher in protein, lower in ratios of car- bon to nitrogen, probably more rapid digestion kinetics) than diets of deposit feeders. We suggest that polychaete species with simple, tubular guts and relatively large ratios of body volume to gut volume (B/G > 7) are more likely to be carnivores than deposit feeders.

Polychaetes exhibit the same general patterns in gut ar- chitecture that are seen among other animal groups. Among mammals, for example, carnivores have simple guts while herbivores have more elaborate guts, and relative gut vol- ume decreases with increasing diet quality (Hume 1982). Gut masses in mammalian carnivores tend to be smaller than gut masses in similarly-sized ruminants (Calder 1984), and, among the ruminants, the weight of the reticulo-rurnen and contents (together about 80% of the total weight of the gut and contents) decreases relative to body weight as diet quality increases (Hoppe 1977).

In the context of digestion theory we can generalize observed relationships between gut architecture and diet quality and modify Sibly's prediction of increasing relative gut volume with decreasing food quality as applied to simi- larly sized animals. An increase in gut volume that results in an increase in throughput time should occur when food quantity becomes limiting, i.e., an animal should increase extent of digestion (Jumars and Penry 1988). An increase in gut volume with no corresponding increase in throughput time should occur when food quality is limiting, i.e., an animal should maximize production rate of digestive prod- ucts. This latter response has been observed in laboratory experiments with birds (Savory and Gentle 1979; A1- Joborae 1980).

Food quality rather than quantity is likely to be limiting for deposit feeders, and deep-sea deposit feeders are thought to have, on average, diets lower in quality than nearshore , and shelf deposit feeders (Carney 1989 and references there- in). They have more gut volume per unit of body volume and relatively longer guts than nearshore and shelf deposit feeders when comparisons are restricted to closely-related species within a gut-architecture group (to make it more likely that the species compared have similar digestive kine- matics). Based on the arguments above and those of Dade et al. (in press), we would predict that deep-sea deposit feed- ers should have throughput times similar to those of near- shore and shelf species and should digest and absorb in- gested organic matter to the same or relatively greater ex- tents. As Carney (1989) emphasizes, however, measure- ments of the types of sedimentary organic matter utilized by deposit feeders and the pathways, rates and extents of utilization are essentially nonexistent. Deposit feeders may not be constrained by average food quality but may key in on pulses of relatively higher-quality organic matter (e.g., Khripounoff and Sibuet 1980; Smith and Baldwin 1984; Gooday/988; Jumars et al. 1989; Lochte and Turley/988).

Even at this relatively general level of comparison, deep-sea versus nearshore and shelf deposit feeders, the current in- ability to quantify food resources and digestive kinematics limits understanding.

Gut architecture and digestive and foraging constraints

Digestion theory allows us to suggest reasonable digestive kinematics and foraging constraints for deposit-feeding polychaetes with simple, tubular guts, a gut architecture that is very common among deposit feeders. We predict and have so far found that the guts of these species operate as plug-flow reactors (no axial or radial mixing of sediment particles within the gut; Penry and Jumars 1986, 1987; Penry 1989). Advantages of a simple gut for a deposit feeder are that it may be relatively inexpensive to construct and maintain, and rapid growth and reproduction may be char- acteristics of many of these polychaetes (e.g., Armandia spp., Woodin 1974; Capitella eapitata, Grassle and Grassle 1974; Streblospio benedicti (Spionidae), Levin et al. 1987).

Among mammals simple guts indicate short throughput times and relatively high-quality diets (Hume 1982). A sim- ple, tubular gut similarly may allow deposit-feeding poly- chaetes to process rapidly large amounts of material, but may limit these worms to exploiting relatively higher-quali- ty foods - to feeding on surface flocs, inhabiting areas of organic enrichment, or having feeding strategies that incor- porate significant degrees of carnivory or herbivory. Several species that we examined, Capitella cf. capitata, Tharyx multifilis, Cirratulus cirratus, Chaetozone cf. setosa, Para- prionospio pinnata, Levinsenia oculata, are characteristic of areas of organic enrichment or have been shown to respond rapidly to organic enrichment (Pearson and Rosenberg 1978; Fauchald and Jumars 1979; Smith 1986; Weston, pers. comm.). In fact, many "opportunistic" deposit feeders belong to three polychaete families, Capitellidae, Cirratuli- dae and Spionidae (Pearson and Rosenberg 1978), that are characterized by simple, tubular guts. There is evidence that carnivory may be important in the feeding strategies of at least two of the "deposit-feeding" species that we exam- ined (Levinsenia oculata, Fauchald and Jumars 1979; Eucly- mene reticulata. Penry, pets. obs.). Nearly nothing is known about the ecology of two sessile, deep-sea deposit feeders with tubular guts, Tharyx luticastellus and Fauveliopsis gla- bra; T. luticastellus is a surface deposit feeder, and F. glabra probably is. T. luticastellus lives in an elaborate mud con- cretion that may induce local deposition on the sediment surface (Jumars 1975), and bacterial standing stocks are enhanced around those concretions that are occupied by worms (Thistle and Eckman 1990). It is further distin- guished as having by far the highest fraction of body vol- ume occupied by gut of any polychaete we have examined so far and thus may achieve a relatively high throughput time with a relatively high throughput rate. We suspect that Fauveliopsis will be found to have an unusual feeding ecology, perhaps supplementing its apparent sediment diet with richer foods.

The potential limitations imposed by relatively short throughput times and the need to ingest relatively high- quality foods are not necessarily the only, or even the most important, constraints on foraging and digestion in all de- posit feeders with simple, tubular guts. Our results suggests that there may be an upper limit on body size in deposit-

feeding polychaetes with such simple, tubular guts (Table 3). It may reflect general, evolutionary body size constraints resulting from selection for relatively rapid growth and re- production, or it may reflect digestive constraints. Smaller individuals have a digestive diffusion advantage and can obtain digestive products at greater rates (Dade et al. 1990). As we have noted (Penry and Jumars 1987) small deposit feeders with simple, tubular, plug-flow guts dominate areas of organic enrichment and the relatively food-poor deep sea environments characterized by sediments of low per- meability (i.e., muds). Additional digestive limitations im- posed by the permeability of ingested sediments on diffu- sion of enzymes and digestive products may also have con- strained polychaetes that ingest mud to decrease gut diame- ter relative to gut length (i.e., to increase gut aspect ratio) while maintaining similar proportions of gut volume to body volume as they grow.

It is difficult to suggest general digestive constrains for deposit feeders with compartmentalized guts. Similarities in gut architecture do not necessitate similarities in digestive processes. We know, for example, that axial mixing is im- portant in the guts of two ampharetids, Hobsonia florida and Amphicteis scaphobranchiata (Self and Jumars 1978; Penry 1989). They and other terebellimorphs (Dales 1955) have compartmentalized guts that can be modeled as mixing reactor/plug-flow reactor series (Penry 1989). Abarenicola pac~'ca and A. vagabunda also have compartmentalized guts, but they operate as plug-flow reactors (Penry and Jumars 1987; Plante et al. 1989). Travisia foetida has an elaborate and unusual gut (Penry 1988), and we suspect that microbial fermentation may be important in its di- gestive strategy - an hypothesis also suggested by the char- acteristic smell of the species that is" reflected in its name. Experimental descriptions of digestive kinematics (e.g., Penry 1989) are necessary prerequisites to identification of foraging and digestive constraints among deposit feeders with compartmentalized guts.

Ontogenetic changes in gut architecture

Within-species analyses of gut parameters are less likely to be affected by our lack of knowledge of gut kinematics. In the majority of the species we examined gut volume remains a constant proportion of body volume as body volume increases. Gut volume is a linear function of body volume - rather than a power function of body volume with an exponent less than one as suggested by Forbes and Lopez (1987) for Capitella sp. I. They, however, in- ferred trends in gut volume from patterns of gut fullness instead of measuring gut volume directly. Degrees of gut fullness affect gut volume estimates since polychaete guts are very distensible, and worms with relatively less full guts do not necessarily have relatively less gut volume as Forbes and Lopez implicitly assume.

In general the scaling of throughput rate with body vol- ume (or mass) parallels the scaling of metabolic rate with body volume (or mass). Both rates scale as power functions of body volume with exponents less than one - generally between 0.67 and 0.75 (Calder 1984). Forbes and Lopez (1987) found that egestion rate scales as body volume to the 0.70 power for Capitella sp. I, and in an among-species comparison of ingestion rates of deposit feeders Cammen (1980) found that ingestion rate scales as body mass to

10

the 0.77 power when the fraction o f organic mat te r in the food is removed as a covariable. Since gut volume scales as body volume to a power greater than 0.7 - it, in fact, scales as body volume to a power of one - th roughput t ime must increase as body size increases. Extent of diges- t ion is completely determined by th roughput time (Penry and Jumars 1987), and thus extent of digestion must in- crease with body size in deposi t feeders (if diet and digestive react ion kinetics remain more or less constant).

These relat ionships suggest that digestive processing constraints may be more impor tan t in small individuals o f deposit-feeding species than they are in large individuals. Supply-side opt imizat ion arguments appl ied to metabol ism suggest that smaller individuals have higher weight-specific metabol ic demands because they have higher weight- specific rates of metabol ic gain (Dade et al., in press). The diffusion advantage o f small individuals may yield greater absorpt ive rates of digestive products , but they may also have relatively shorter th roughput times and lower digestive conversions. Thus, if digestive kinetics remain constant , small individuals require relatively high-qual i ty food re- sources to achieve their relatively high weight-specific rates of metabol ic gain. Hatchl ing and juvenile iguanas have the same digestive capacit ies (same B/G's) as adults, but have a mean gut residence time that is about one-hal f that of adults and select foods higher in protein (Troyer 1984).

We suggest that avai labi l i ty of adequate food resources for juveniles may be impor tan t in determining dis tr ibut ions of deposit-feeding species, especially those species with sim- ple, tubular guts. Juvenile Hobsoniaflorida (Ampharet idae) appear to be highly dependent upon the availabil i ty o f benthic d ia toms and compete strongly for them with oligo- chaetes (Gal lagher et al., in press). Mos t research on deposi t feeders, however, has focused on adults, and juveniles can- not be viewed simply as smaller versions of adults. Juvenile Capitella sp. I, for example, have ingestion rates that are significantly higher than would be expected by extrapola t - ing ingestion rates observed in larger worms (Forbes 1989). Theory and observat ion thus suggest that studies of the ecology o f juveniles of species that are deposit-feeders as adults are sorely needed.

Acknowledgements. We thank the Director of Friday Harbor Lab- oratories for the use of the Laboratory's facilities and resources. D.P. Weston, D. Thistle and S.J. Brumsickle provided specimens for dissection, and R.F.L. Self and D. Wethey helped to write the programs for calculating volumes. A.R.M. Nowell, ,I.L Hedges, B.B. Krieger, C.R. Smith, and D.P. Weston provided constructive comments on earlier drafts. Research and publication were sup- ported by contracts from the Office of Naval Research (under N00014-87-K-0160) to P.A. Jumars and A.R.M. Nowell and to B.W. Frost. Contribution 1823 from the School of Oceanography, University of Washington.

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Received April 11, 1989 / Received in revised form August 24, 1989 / Accepted September 26, 1989