Intestine length in the fishes of a tropical stream: 2. Relationships to ...

Environmental Biology of Fishes 42: 129-141,1995. O 1995 Kluwer Academic Publishers. Printed in the Netherlands

Intestine length in the fishes of a tropical stream: 2. Relationships to diet - the long and short of a convoluted issue

Donald L. Kramer & Michael J. Bryant' Department of Biology, McCill University, 1205 Docteur Penfield Avenue, Montreal, Quebec H3A 1 BI, Canada ' Present address: Department of Biology, University of California, Riverside, CA 92521, U.S.A.

Received 3.8.1993 Accepted 8.6.1994

Key words: Alimentary tract, Carnivore, Central America, Digestive system, Feeding habits, Food, Fresh- water fish, Herbivore, Omnivore, Neotropics, Panama, Stream ecology

Synopsis

We examined the relationship between the intestine length and the amount of plant material in the diet of 21 species of fish from forest streams in Panama. Alimentary tract analyses supplemented by literature reports showed that four loricariid catfish species and one poeciliid were specialized herbivores consuming almost exclusively periphyton and detritus. Four species, including one erythrinid, one characid, one trichomyctycte- rid and one eleotrid, were carnivores consuming almost entirely food of animal origin. Twelve species, including five characids, one lebiasinid, two pimelodelids, three cichlids and one poeciliid, were omnivores consuming food of both plant and animal origin, but the average proportion of food of plant origin (detritus and algae plus higher plant parts) varied from 4-60%. Most omnivores increased plant food consumption with increasing size. Because intestine length increases allometrically with body size and the pattern of increase differs considerably among species and is influenced by 1ength:mass relationships, we compared species at the same size and took both length and mass into account. At a given size, intestine lengths of herbivores were longer than those of omnivores, and these were longer than those of carnivores. Differences in intestine length among the dietary categories were greater at larger body sizes and when the common size was defined by body mass than when it was defined by body length. There was no trend for the average proportion of plant material consumed to be related to intestine length among the omnivores, when confounding effects of body mass were taken into account. The slopes of the allometric equations relating log,, intestine length to log,,, body size for herbivores tended to be higher than for omnivores and higher for omnivores than for carnivores, but both herbivores and omnivores showed extensive variation and overlap with the other dietary categories. Among the omnivores, there was no trend for slopes to be steeper for species consuming more plant material on average or for species showing larger ontogenetic increases in plant consumption. These results permit increased precision in describing diet-intestine length relationships, but indicate that the widely held belief that intestine length reflects diet in fishes should only be applied to broad dietary categories and not to finer divisions among omnivores.

Introduction

In many vertebrate taxa, herbivorous species tend to have longer intestines than do carnivorous species (e.g. lizards: Skoczylas 1978; birds: Leopold 1953; mammals: Chivers & Hladik 1980; Schieck & Millar 1985). For fishes, this pattern is reported in many textbooks and reviews (e.g. Barrington 1957, Norman & Greenwood 1963, Nikolsky 1963, Lagler et al. 1977, Fange & Grove 1979, Moyle & Cech 1982, Horn 1989, Wootton 1990). This view is based largely on reviews of digestive system morphology that provide ratios of alimentary tract length to body length for fishes in different dietary categories (Al-Hussaini 1947, Kapoor et al. 1975) and on se- lected comparisons of related species with different diets (Al-Hussaini 1949, Fryer & Iles 1972, Kline 1978). Surprisingly, there have been few attempts to describe quantitatively or to evaluate statistically the strength of the association between herbivory and intestine length in fishes. A more precise quantification of the relationship between diet and intestine length would appear to be a prerequisite to understanding the functional significance of interspecific differences in digestive system morphology and development. In addition, such quantification might permit approximate trophic position of a species to be assessed by a simple morphological mea- surement.

Available data suggest that the relationship between diet and intestine length is far from consistent (Horn 1989). The ranges of relative intestine lengths (intestine length divided by body length) for fishes in different dietary categories are fre- quently broad and overlapping. For example, relative intestine lengths summarized by Al-Hussaini (1947) and Kapoor et al. (1975) range from 0.5 to 2.4 for carnivores, 0.8 to 4 for omnivores, and 2 to 21 for herbivores. In a comparative study of Caribbean Pomacentridae with a broad range of diets, Emery (1973) was able to find 'no specific relationship' between the intestine length and the amount of plant material in the stomach [but see Montgomery (1977)l. Goldschmid et al.'s (1984) comparable study of Blenniidae from the Adriatic Sea revealed a weak, though significant, correlation between percent algae in the diet and relative intestine

length, with a number of striking exceptions. In a stream-dwelling fish community from the south- eastern U.S.A., Ribble & Smith (1983) found a weak, significant correlation between relative intestine length and a diet index based on literature reports, but the correlation was non-significant when the index was based on the actual stomach contents of their specimens.

The variability, weakness and inconsistency of the relationships could be a consequence of the measure of intestine length used. Most studies have considered only relative intestine length despite the fact that this measure often increases with body size (e.g. Klust 193911940, Hiat 1944, Odum 1970, Braber & De Groot 1973, Emery 1973, Naiman 1975, Mont- gomery 1977, Kline 1978, Zihler 1982, Ribble & Smith 1983, Lassuy 1984). In an analysis of 21 species of fishes from a Neotropical stream community, Kramer & Bryant (1995) concluded that most species showed positively allometric relationships between intestine length and body size. Thus, some of the variability in previous studies could have arisen through the use of relative intestine length to compare species of different sizes. Furthermore, in the species studied by Kramer & Bryant (1995) heavier species tended to have longer intestines when compared at a common length and longer species tended to have shorter intestines when compared at a common mass. Thus, failure to take body mass differences into account could be another source of variability.

The present study examines the quantitative relationship between diet and intestine length for the fish community whose intestinal tract allometry was analysed by Kramer & Bryant (1995). Because of large interspecific differences in both the coeffi- cient and exponent of the intraspecific allometric relationships, it was not possible to devise a valid scaling formula to compare species when the sizes of the measured individuals differed. To reduce ex- traneous sources of variability, we therefore compared species only at a common size using the allometric equations obtained in the previous study and took into account the effects of interspecific differences in body mass at a common body length. In addition, we considered whether the exponent of the allometric equation, i.e. the rate at which intes-

tine length increased with body size, was related to diet type or to ontogenic changes in diet. The community we studied included species with wide variation in diet, ranging from piscivores to periphyton and detritus grazers, with many omnivorous species including in their diets terrestrial and aquatic invertebrates, algae, and allochthonous plant material (fruit, seeds, leaves, and flowers) from the sur- rounding forest. Many of these species include mix- tures of varying proportions of these different com- ponents. This provided an opportunity to examine whether intestine length varied only in relation to broad dietary categories or whether it reflected the quantitative composition of the diets of the omnivorous species.

Materials and methods

The study was based on 21 species of fishes from forest streams in Panama for which a sufficient size range was collected to permit analysis of intestine length (mm) and body size [standard length (SL) in mm, body mass (M) in g] allometry by Kramer & Bryant (1995). The fish community and sites were described by Kramer (1978), Angermeier & Karr (1983), Power (1984) and Kramer & Bryant (1995). Fish were collected primarily by seines; some specimens were obtained using traps and a single rote- none collection. Collections were made between November 1973 and July 1975 and during May and June 1979, covering all periods of the year but with a relatively large proportion from the late dry and early rainy seasons (April-May). Specimens were placed on ice as soom as captured and kept chilled or frozen until examined. Because collections also were used for other studies, not all measurements were available for all specimens.

For diet analysis, only the stomach contents were considered for most species. For fish without stomachs the anterior intestine up to the first bend was used. For fish that were infrequently captured or in which the stomach was often empty, recognizable items in the rest of the intestine were also considered. This was particularly important for the cichlids in which the anterior intestine often con- tained food when the stomach was empty. Food

items were categorized under a dissecting micro- scope, and the percent contribution to the total vol- ume of contents was estimated visually. Categories were (1) sediment particles, (2) detritus, (3) unicellular and filamentous algae, (4) leaves and flowers of terrestrial plants, (5) seeds and fruits of terrestrial plants, (6) terrestrial invertebrates (insects and spiders), (7) aquatic invertebrates (mostly aquatic insects, but some gastropods, decapod crustaceans and rhizopods, (8) fish, (9) fish scales, and (10) other or unidentifiable. Because many of the characoid fishes forage in groups and bite off small pieces of larger items, separation of terrestrial and aquatic insects and recognition of fruit or seeds was sometimes uncertain. The mean percentage of each category was calculated for each species, giving equal weight to all individuals. For the quantification of herbivory, categories 1-5 were added together. To examine whether the degree of herbivory changed with size, all specimens of a species were partitioned into equal logarithmic size classes (log,, M =

- 1.0001-0.0000, 0.0001-1.0000 and 1.0001-2.0000), and a Kruskal-Wallis test (SAS Institute Inc. 1985) was used to determine whether there were significant differences in percent plant matter between any size classes containing at least 4 specimens. Be- cause dietary information was based on relatively small sample sizes for some species and on sampling that was limited in time and space for all species, conclusions were augmented by published data on the same and closely related species from the same and other stream systems.

Kramer & Bryant (1995) give the methods for intestinal measurements and analyses and provide (Appendices 1-3) parameters for the reduced major axis regressions of body mass on body length and of intestine length on body length and body mass. To examine the size-specific relationships among diet. intestine length, and body size, we se- lected three sizes at equal (logarithmic) intervals that spanned our data set (log,, SL = 1.4,1.7, and 2.0, approximately 25, 50, and 100 mm, and log,,, M =

- 0.5, 0.5, and 1.5, approximately 0.3, 3, and 30 g). We used the morphometric regressions to calculate the expected mass and intestine length at each standardized body length and the expected body length and intestine length at each standardized body mass

for each species, but only over the range of sizes of specimens which had been used in calculating the regressions. At each of the standardized body lengths and body masses, we then examined the partial correlations between percent plant material in the diet (subjected to angular transformation) and intestine length and between the alternative size measure and intestine length. Species which had both plant and animal material in their diet were only included in the correlations if we had diet samples from at least four individuals of that size category.

Results

Diets

The diet summaries (Table 1) indicate that the 21 species of fish can be divided into three broad categories. The intestines of all four species of loricariid catfishes and Poecilia, which we refer to as 'herbivores', were typically filled with a mixture of benthic algae, detritus and sediment particles which indicate periphyton grazing. Although sample sizes for this group are small because they were the focus of other investigations, qualitative observations during our numerous intestinal measurements indicated that this was a consistent pattern. Our results also match those of other workers in this and other systems (Breder 1927, Angelescu & Gneri

Table I . Average composition of alimentary tract contents of 21 genera and species of freshwater fish from Panama.

Speciesa Nb Size Mean Diet (%)d rangec

Min. Detr. Alg. Leaf. Fruit T. inv. A. inv. Fish Scale Other

a. Ancistrus b. Chaetosroma C. Hypostomus d. Poecilia e. Rineloricaria f. Brycon p. g. Brycon c. h. Bryconamericus i. Cichlasoma j. Aequidens k . Geophagus I. Brachyraphis m. Piabucina n. Pimelodella o. Rhamdia p. Hyphessobrycon q. Gephyrocharax r. Trichomycterus s. Roeboides t. Gobiomorus u. Hoplias

": Species listed in descending order of percent food of plant origin. b: Number of specimens examined. ': Standard length (mm). d: Abbreviations for diet categories are: Min = mineral particles, Detr. = terrestrial macrophyte detritus, Alg = unicellular and filamentous algae, Leaf. =fresh terrestrial leaves and flowers, Fruit =fresh terrestrial fruits and seeds, T. inv. =terrestrial invertebrates, A. inv. = aquatic invertebrates, Fish =remains of ingested whole fish, Scale =fish scales without other evidence of ingested fish, Other = unable to identify or not fitting other categories. ': Value includes Min, Detr, and Alg grouped together.

Table2. The mean percent plant material (including sediment, detritus, algae, and terrestrial plant categories) for three size classes of 12 species of omnivorous fish from streams in Panama. Also shown is the slope of the log,,, intestine length: log,,,standard length relationship from Kramer & Bryant (1995).

Species"

Percent plant material

Smallb Intermediate Large Mean xZ * P Slope

Brycon p. Brycon c. Bryconamericus Cichlasoma Aequidens Geophagus Brachyraphis Piabucina Pimelodella Rhamdia Hyphessobrycon Gephyrocharax

" Presented in order of decreasing mean amount of plant material. Size classes [Mass (M) in g]: small = log,,, M = - 1.&0.0; intermediate = log,,, M = 0.1-1.0; large = log,,, M = 1.1-2.0. Sample size in parentheses. Data are presented for a size class only if sample size was 2 4.

* Chi square approximation of the Kruskal-Wallis test statistic for differences in percent plant material among size classes.

1949, Saul 1975, Angermeier & Karr 1983, Power 1984). The only exception to this trend was the presence of significant numbers of insect larvae in the intestines of two very small Rineloricaria (25 and 27 mm), suggesting a partially insectivorous diet. Similar observations in the same system were reported by Pineda (1976, cited by Power 1984) and have also been noted for related species in Argenti- na (Angelescu & Gneri 1949). Our limited quantitative and numerous qualitative observations sug- gested that such insect consumption did not occur in larger individuals of Rineloricaria or at any size in the other loricariid species. The only occurrence of invertebrate consumption in Poecilia occurred during an experiment in which large amounts of frozen brine shrimp Artemia were supplied to the stream (D.L. Kramer unpublished observations). Because the documented invertebrate consumption in Rine- loricaria appeared to occur only in extremely young individuals and in Poecilia only under artifical cir- cumstances, we retained these species in the 'herbivore' grouping.

The majority of species in this system had significant, though variable, amounts of both plant and animal material in their diets over most of the size

range sampled and were therefore classed as 'omnivores'. The average amount of food of plant origin in the diet ranged from 59.5% for Brycon petrosus to 4.2% for Gephyrocharax (Table 2). Plant material included a wide range of fruit, seeds, leaves and flowers from the trees overhanging the stream, as well as filamentous and unicellular algae mixed with detritus and sediment from the substrate. Pisci- vory was rare among the omnivores; items of animal origin included primarily benthic invertebrates, especially insect larvae, and terrestrial insects such as ants and grasshoppers which fell into the stream. There were large differences among species in the relative use of these different items. Many of the omnivorous species were categorized as aquatic insectivores or general insectivores rather than omnivores by Angermeier & Karr (1983) who studied them in the same and nearby streams. Although our observations agree with regard to the general importance of aquatic versus terrestrial insects, we recorded considerably more plant material (Table 2). In Cichlasoma we found 42% of the gut contents consisted of detritus and algae whereas Angermeier & Karr (1983) reported none; in Ae- quidens our figure for detritus plus algae was 19%

while they reported less than 1%; in Brachyraphis cascajalensis it was 21% as compared to 2%; in Ge- ophagus we found 15% terrestrial plant material as compared to none; and in Rhamdia 10% as compared to 3%. Only for Piabucina was there an oppo- site trend; we found about 12% terrestrial plant matter and 6% algae and mineral particles, whereas Angermeier & Karr (1983) reported figures of 20% and 19%, respectively.

There was a strong tendency for the omnivores to increase their use of plant material with increasing size (Table 2). Such increases were statistically significant in Bryconamericus, Brycon chagrensis, Brycon petrosus, Pimelodella and Geophagus and nearly significant in Piabucina and Aequidens. Al- though the change in Hyphessobrycon was not significant and the amount of plant material was small, stomachs of fish in the intermediate size class had on average more than twice as much plant matter as those in the small size class. Since sample sizes were inadequate to make comparisons between size classes for Cichlasoma and Rhamdia and were limited in Brachyraphis, the only species which clearly failed to show a trend for increased herbivory with increased body size was Gephyrocharax, the least herbivorous of the omnivores. Angermeier & Karr (1983) reported increased herbivory with size in all species in which we found significant or borderline trends with the exception of Geophagus and Piabu- cina, although their Bryconamericus sample was mixed with Astyanax ruberrimus and the two Bry- con species were combined in their data set.

The four species we refer to as 'carnivores' consumed almost exclusively material of animal origin. Hoplias and Gobiomorus typically preyed on other fishes and large invertebrates. Our rather sparse samples are confirmed by other studies of these widespread genera (Breder 1927, Zaret & Rand 1971, Saul 1975, McKaye et al. 1979, Angermeier & Karr 1983). Trichomycterus fed almost exclusively on benthic aquatic invertebrates, mainly insect larvae. The fourth carnivorous species, Roeboides, fed both on benthic invertebrates and on scales taken from other fish as found by Angermeier & Karr (1983) and reported in studies of congeners from other localities (Sazima 1983, Sazima & Machado 1982).

Intestine length

When considered at standardized body lengths, relative intestine lengths overlapped only slightly among the dietary categories (Fig. 1, Table 3A). In the small length class relative intestine length ranged from 0.6-1.4 among omnivores and 1.2-9.3 among herbivores (there were no data for carnivores in this size class). In the intermediate length class, carnivores ranged from 0.6-0.8, omnivores from 0.7-1.7 and herbivores from 2.5-16.4. In the large length class there was no overlap between dietary categories: carnivores 0.7-0.9, omnivores 1.1-2.2, herbivores 5.4-28.7. Zihler's Index (intestine length divided by 10 M ' I 3 (Zihler 1982)) overlapped even less than relative intestine length. With increasing size, the upper and lower limits and total range of both relative intestine length and of Zih- ler's Index increased within each dietary category (Fig. 1, Table 3B).

Relationships between intestine length and plant material in the diet appeared to be due exclusively to differences between large dietary categories rather than to any effect of the degree of herbivory among the omnivores, once the effects of species differences in body mass for a given body length were taken into account. When all species were included, correlations between intestine length and percent plant material in the diet were highly significant for all three size classes (Table 4). For size standardized by body length, body mass had a significant partial correlation with intestine length in the small and intermediate length classes (Table 4A), but when size was standardized by body mass, body length was uncorrelated with intestine length in two size classes and only marginally correlated in the small size class (Table 4B). Because the specialized algae-grazing herbivores were clearly outliers in these relationships (Fig. I), we analyzed the relationships between intestine length and percent plant material in the diet without the herbivores (Table 4Aii, Bii). Using both length and mass to standardize size, there was a significant correlation between intestine length and plant material in the diet for the intermediate and large size classes. In the small size class, there was no correlation. When carnivores were also excluded so that the compari-

Size-specific percent plant Size-speciflc percent plant

Fig. I. The relationship between intestine length and percent of plant material in the diet at (a, b, c) three standard body lengths (log,,, SL = 1.4,1.7, and 2.0, approximately 25.50, and 100 mm, respectively) and (d, e, f) three standard body masses (log,,, M = - 0.5,0.5, and 1.5, approximately 0.3,3, and 30 g, respectively) for 21 species of tropical freshwater fishes. Note the angular transformation of the abscissa and the log,,, transformation of the ordinate. Each species is represented only at sizes included within the range of specimens measured. Herbivores are indicated by triangles, omnivores by dots and carnivores by circles.

son involved only the omnivores (Table 4Aiii, Biii), tween intestine length and plant material in the diet there was no effect of percent plant material in the for any size class of omnivores (Table 4B). diet on intestine length in any length class. How- There was a tendency for slopes of the log,, in- ever, in the intermediate and small length classes, testine length:log,, body size relationships to be low intestine length did have a significant partial corre- for carnivores and higher and more variable in om- lation with body mass. When size was standardized nivores and herbivores, but with extensive overlap by mass, there was no detectable correlation be- (Fig. 2). For the relationship between intestine

length and standard length, slopes ranged from

Table 3. Absolute intestine length (mm) and relative intestine length of 21 species of freshwater tropical fish at (A) three body lengths (mm) and (B) three body masses (g) predicted by regression equations from Kramer & Bryant (1995). Values are only provided within the range of specimens actually measured. Relative intestine length (RIL) is intestine lengthlstandard length. The Zihler index (ZI) follow- ing Zihler (1982) is intestine lengthll0 (mass)"'. Omnivores are presented in order of decreasing herbivory. The standardized standard lengths are small (S) = log,, (SL) = 1.4; intermediate (I) = log,, (SL) = 1.7; large (L) = log,, (SL) = 2.0. Standardized masses (M) are log,, (M) = - 0.5,0.5, and 1.5, respectively.

A. Intestine length at standard body lengths B. Intestine length at standard body masses.

IL(mm) RIL

S I L S I L

IL (mm) ZI

S I L S I L

i. Herbivores a. Ancistrus b. Chaetostoma c. Hypostomus d. Poecilia e. Rineloricaria ii. Omnivores f. Brycon p. g. Brycon c. h. Bryconamericus i. Cichlasoma j. Aequidens k . Geophagus 1 . Brachyraphis m. Piabucina n. Pimelodella o. Rhamdia p. Hyphessobrycon q. Gephyrocharax iii. Carnivores r. Trichomycterus s. Roeboides t . Gobiomorus u. Hoplias

i. Herbivores a. Ancistrus b. Chaetostoma C . Hypostomus d. Poecilia e. Rineloricaria ii. Omnivores f. Brycon p. g. Brycon c. h. Bryconamericus i. Cichlasoma j. Aequidens k . Geophagus 1 . Brachyraphis m. Piabucina n. Pimelodella o. Rhamdia p. Hyphessobrycon q. Gephyrocharax iii. Carnivores r. Trichomycterus s. Roeboides t. Gobiomorus u. Hoplias

1.36-2.11 for the herbivores, 1.15-2.01 for the omnivores, and 1.09-1.28 for the carnivores. For the relationship between intestine length and body mass, the equivalent values were 0.39-0.66 for herbivores, 0.38-0.65 for omnivores, and 0.35-0.40 for carnivores. An analysis considering all species showed that there was a positive correlation between slope of the log,, intestine length: log,, body size relationship and the percent of plant material in the diet (for log,, IL: log,, SL slope vs. percent plant: r =

0.67, p = 0.0009; for log,, IL: log,, M slope vs. percent plant: r = 0.64, p = 0.002). However, the effect appeared to be primarily due to the herbivore cate-

relation coefficients decreased and became non- significant (log,, IL: log,, SL: r = 0.27, p = 0.31; log,, IL: log,, M: r = 0.36, p = 0.17). When only the omnivores were considered, the correlations were even lower (log,, IL: log,, SL: r = - 0.09, p = 0.78; log,, IL: log,, M: r = 0.003, p = 0.99).

Because many of the omnivores increased their consumption of plant material as they grew larger, it was possible that slopes of the intestine length: body size relationship might reflect the degree to which the diet changed with size. However, we found no evidence of such a relationship (Table 2). Pimelodella chagresi, the omnivorous species with

gory. When the herbivores were removed, the cor- the steepest slope (2.01) increased plant consump-

Table 4. Correlations between intestine length and percent plant material in the diet for 21 species of tropical freshwater fish at three standard sizes. In Part A, standardized log,, standard lengths are used (small (S) =log,, (SL) = 1.4; intermediate (I) = log,, (SL) = 1.7; large (L) = log,,, (SL) = 2.0) and mass is used as an independent variable in a partial regression analysis. In Part B standardized log,masses are used ((M) are log,, (M) = - 0.5,0.5, and 1.5) and length is used as an independent variable. Species are only used if measurements of intestine length and diet were made in the appropriate range; n indicates number of species for a given comparison.

A. Standardized length

i. All species Percent plant Mass

Size n R~ p Partial r2 p Partial r2 p

S 12 0.89 0.0001 0.50 0.01 0.39 0.0003 I 17 0.86 0.0001 0.82 0.0001 0.04 0.017 L 10 0.79 0.004 0.72 0.002 0.07 0.16 i i Omnivores and carnivores s - - - - - - -

I 12 0.88 0.0001 0.14 0.009 0.74 0.0003 L 7 0.710.08 0.58 0.05 0.13 0.25 iii. Omnivores only S 9 0.60 0.07 0.004 0.81 0.59 0.02 I X 0.74 0.03 0.09 0.23 0.65 0.02 L 5 0.33 0.67 0.15 0.52 0.18 0.54

B. Standardized mass

i. All species Percent plant Mass

Size n R2 p Partial r2 p Partial r2 p

S 13 0.88 0.0001 0.81 0.0001 I 17 0.86 0.0001 0.86 0.0001 L 9 0.77 0.01 0.76 0.002 ii. Omnivores and carnivores S 10 0.52 0.07 0.00 0.98 I 12 0.69 0.006 0.68 0.0009 L 7 0.67 0.11 0.67 0.03 iii. Omnivores only S 8 0.34 0.35 0.005 (-) 0.85 I 8 0.11 0.74 0.11 0.42 L 5 0.30 0.70 0.28 0.36

Percent plant in the diet Fig. 2. Relationship between slopes of the log,, intestine length:log,,, body size relationships and the percent plant material in the diet for 21 species of tropical freshwater fish. Figure shows slope (f 95% confidence interval) for each species where (a) standard length and (b) mass were used for the calculation of intestine length allometry. Herbivores are indicated by triangles, omnivores by dots and carnivores by circles. Small letters next to each symbol identify individual species as listed in Table I. Dashed lines indicate isometric slopes of 1.0 for standard length and 0.33 for mass. Note the angular transformation of the abscissa.

tion from 0 to about 20% but three species that increased from 0 to about 30% had much lower slopes (Aequidens coeruleopunctatus 1.16, Geophagus crassilabris 1.20, and Piabucina panamensis 1.18), and Bryconamericus emperador with a much more dramatic change of 14-98% had a similar slope of 1.23 as did Brycon petrosus with an increase of 24- 75% and a slope of 1.20. On the other hand, Gephy- rocharax atricaudata (1.46) and Brachyraphis cascajalensis (1.61) had steeper slopes although they did not show detectable changes in diet with size. Since the slopes of the log,, intestine length:log,, body mass relationships are closely correlated with the slopes of the log,, intestine length:log,, body length relationships (Kramer & Bryant 1995), considera- tion of slopes using the mass-based relationships gave the same result.

Discussion

In a tropical stream fish community, we found that the relative intestine lengths of periphyton-grazing herbivores were in general larger and more variable than those of omnivores, which in turn were larger and more variable than those of carnivores. These findings broadly parallel those for other systems such as the fishes of the Red Sea (Al-Hussaini 1947), cichlids of the Great Lakes of Africa (Fryer & Iles 1972, Reinthal1989), fishes of a North Amer- ican stream (Ribble & Smith 1983), and blennies of the Adriatic Sea (Goldschmid et al. 1984).

As in other comparative surveys (Kapoor et al. 1975), relative intestine lengths of fish representing dietary categories overlapped considerably. How- ever, this overlap was nearly eliminated when only fish of the same length or mass were compared. This suggests that some of the variation in previous investigations may be due to variability in the size of fish considered. In all dietary categories, both maxi- mal and minimal values for relative intestine length tended to increase with body size, but the absolute increase was much greater for the herbivores than for the omnivores and greater for the omnivores than the carnivores. This overall pattern can be seen in the plots of the regression lines for each species (Kramer & Bryant 1995, Fig. 2). Thus, future

comparisons of intestine length should standardize the sizes at which fish are compared.

Our study also indicates that interspecific differences in 1ength:mass relationships are another confounding variable in comparative studies of intestine length. For correlations at a standardized size, body mass sometimes explained more of the variation in intestine length than percent plant material in the diet did. The reverse effect, length as a partial correlate when comparisons were made at a standardized body mass, was much weaker and only marginally significant in two comparisons. In addition, the separation among dietary categories was much stronger when intestine lengths were compared using the mass-based Zihler Index than the length-based relative intestine length. Therefore, we propose that future studies should use mass rather than length as the base for comparisons wherever possible.

Although the sample sizes are small and the species diversity low, the consistency of the Zihler In- dex suggests that it could be used to identify the general dietary category of fish specimens in the absence of information on stomach contents. Such categorizations might be useful for preserved specimens in which the stomachs are empty or the contents well digested or poorly preserved. Further- more, the intestine length should integrate over larger spatial and temporal scales than would the gut contents at the time of capture. Based on present results, we propose that for a 0.3 g fish, a Zihler Index of 10-35 should indicate a periphyton-grazing herbivore, 2.5-4.5 an omnivore, and 2.2-2.5 a carnivore. For a 3.0 g fish, the figures would be 12-55, 3.5-6.0 and 2.4-3.5, and for a 30 g fish 50-100,4.0- 10.0 and 2.5-3.5. Further work will be required to refine these measurements and extend them to a wider range of species and dietary categories, such as macroalga browsers (Horn 1989).

The lack of any relationship between percent plant material in the diet and intestine length among the omnivores was very clear, despite quite large differences in their diets. Several explanations are possible. It may be that the functional advan- tage of gut elongation for herbivory only applies to the broad dietary category and not to its finer composition. However, it is also possible that our diet

samples failed to adequately describe the omnivorous species, because their diet varies strongly with locale or season. For some species, the level of herbivory which we observed differed strikingly from that reported by Angermeier & Karr (1983) for specimens collected in the same system. In addition, for omnivores, herbivory is a very heterogene- ous category, with plant matter including single- celled and filamentous algae, seeds, fruits, and leaves, items which may differ considerably in their structural requirements for efficient digestion. There may also be an effect of the type of animal food with fish, soft-bodied insect larvae, and mol- luscs or highly chitinized terrestrial invertebrates all having different requirements. Finally, different species may have different ways of digesting the same material; presence or absence of a gizzard-like stomach, a pharyngeal mill or the ability to achieve very low stomach pH values (Lobe1 1981) might greatly influence the type of intestine required. Thus, it is possible that diet would explain more of the variation in intestine length among omnivores if we had sufficient species to examine the implica- tions of more subtle variation in diet composition or digestive system.

Since the log,, intestine length:log,, body size relationships are very close to linear (Kramer & Bryant 1995), the slope of these relationships represents a size-independent species characteristic. This study examined whether these slopes might be as good or better than intestine length at a given size in correlating with diet, but this was not the case. Al- though herbivores tended to have steeper slopes than omnivores and omnivores steeper than carnivores, there was a great deal of overlap and no clear relationship within the omnivores. Although the loricariid catfishes in our study were all herbivores and had among the steepest slopes in our data set (range 1.81-2.11), the herbivorous Poecilia had a lower slope (1.36) near the median of our data set, and the omnivorous catfish Pimelodella (slope = 2.01) had a steeper slope than two of the loricariids. Similarly, calculations from Angelescu & Gneri's (1949) data yield for loricariids moderately steep slopes (Loricaria anus 1.32, L. vetula 1.25, Hyposto- mus commersoni 1.50, Hypostomus plecostomus 1.46), but indicate that the intestine of the periph-

yton-grazing curimatid characoid Prochilodus lineatus grows almost isometrically (slope = 1.06). Our observations might suggest that carnivores taking large prey such as Hoplias (slope = 1.09) and Gobio- morus (slope = 1.14) have very low slopes in con- trast to species feeding on numerous small items such as invertebrates (e.g. Trichomycterus, slope =

1.28) and invertebrates plus scales (Roeboides, slope = 1.28). But this is not confirmed by Ribble & Smith's (1983) observations in which the piscivo- rous largemouth bass Micropterus salmoides had a slope of 1.25, after conversion to reduced major axis regression, very similar to the invertebrate feeder Percina nigrofasciata (1.23), the species with the shallowest slope in their data set.

An alternative hypothesis is that steep slopes characterize those species that undergo important ontogenetic dietary shifts as proposed by Mont- gomery (1977). Although many of the omnivores in our study did increase their level of herbivory with increased body size, we were unable to detect any relationship between the degree of shift and steep- ness of the slope. However, the patterns of shift were quite variable and the sample sizes by which it was characterized were quite limited in some cases, so it is possible that additional data on more species would clarify these questions.

In comparative studies, statistically significant patterns can be wrongly inferred if species which share characteristics because of a common phylogenetic history are treated as independent data points (Harvey & Pagel 1991). Many previous examin- ations of the relationship between intestine length and diet appear to have attempted to control for phylogeny by restricting comparisons to species within families (Al-Hussaini 1949, Fryer & Iles 1972, Goldschmid et al. 1984). However, this is only a partial solution because within-family relationships could still confound interpretations. While several methods have recently been proposed to deal with the problem of non-independence (Har- vey & Page1 1991), we feel that at present the phylogeny of our species is too poorly known and the number of species too small for such methods to have much power. Nevertheless, we recognize that our conclusion of differences in intestine length between broad dietary categories does depend on pat-

terns in only five herbivorous, twelve omnivorous and four carnivorous species. Because the carnivores are from four very distantly related families they should be relatively phylogenetically independent. The twelve omnivores represent five families; only two species are congenetic, and most differ considerably in diet and morphology. Thus, the omnivore group still represents considerable phylogenetic independence. The herbivores, on the other hand, represent only two families, and four of the five species come from the family Loricariidae. Al- though these loricariids are represented by four genera and both the robust and elongate body forms characteristic of this family, given the appar- ent similarity in diet across the family (Power 1984), there is no doubt that the phylogenetic independence of the herbivore sample is low. Some support for the generality of conclusions concerning the intestine length of the periphyton-grazing herbivores comes from Angelescu & Gneri's (1949) study which provides intestine length measurements for the curimatid Prochilodus lineatus. At 100 mm standard length its intestine length would be 398 mm, close to that of the loricariids which range from 536-2871 mm and above that of the omnivores which reach a maximum intestine length of 212 mm. However, additional investigations of unrelated species with similar diets clearly are needed.

Acknowledgements

Vanessa Kramer, John Kramer and Bill Nowell as- sisted greatly in the collection of the fish. Gilbert Cabana helped with the data compilation and initial analyses. Rob Peters, Jim Grant, Tom Miller, Derek Roff, Robert Vadas, Jr., Ernest Keeley and Ana Rakitin provided helpful commentaries at various stages of the project. The research was supported by a Smithsonian Tropical Research Institute Post- doctoral Fellowship (1973-1975) and Natural Sci- ences and Engeneering Research Council of Cana- da operating grants to D.L.K.

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