The Condorg&279-292 0 The Cooper Ornithological Society 1996

MORPHOMETRY OF THE DIGESTIVE TRACTS OF SOME ’

R. E. RNXLEFS Department of Biology, Universityof Missouri-St. Louis, 8001 Natural BridgeRoad, St. Louis, MO 63121-4499

Abstract. To investigatehow the morphologyof the gut is related to diet and body size, severaldimensions of the digestivetract were obtained for 34 speciesof passerinesfrom Costa Rica and Pennsylvania. Measurementsincluded the length and diameter of the in- testine, length and width of the stomach, thicknessesof the muscle, mucosa, and koilin layersof the stomach,thicknesses of the muscleand mucosalayers of the intestine,number per crosssection and length of intestinal villi, and diameter of the lumen of the intestine. In addition, the total absorbtive surfacearea of the intestine was estimated from several primary measurements.Correlations and regressioncoefficients based on phylogenetically independentcontrasts for the lengthsof the stomachand intestinedid not differ significantly from those based on original measurements. The absorbtive surface area of the intestine and the thicknessesof the muscular and mucosal layers of the intestine were related to the 0.6-0.7 power of body mass; other measurementsexhibited allometric constantsclose to 0.3. Further analyseswere basedupon residualsof measurementsabout allometric regressions.Correlation and principal compo- nents analysis revealed positive correlationsamong intestine length, stomach length, and stomachwidth, and negativecorrelations between intestinal diameter and villus length, on one hand, and the thicknessof the stomach(muscle and mucosa),on the other. Discriminant analysisbased on residualsof gut measurementsseparated species placed in three diet groups:insect, mixed insectand fruit, and mixed insectand seed.Insectivores were distinguishedfrom specieswith mixed diets by having smaller but heavier-walled stomachsand smaller intestines.Fruit-eaters were distinguishedfrom seed-eatersprimarily by having thicker-walled intestines. Key words: Comparativeanalysis; diet; digestive tract;gut morphology; intestine; stomach.

INTRODUCTION diet (Moss 1983, Al-Dabbagh, Jiad, and Waheed The morphology of the digestive tract varies sub- 1987, Ankney and Scott 1988, Ievey and Kar- stantially among vertebrate taxa (Ziswiler and asov 1989, Walsberg and Thompson 1990, Dyk- Famer 1972, McLelland 1979, Stevens 1988). stra and Karasov 1992, Hammond and Dia- Certain attributes of the design of the gut differ mond 1992, Piersma, Koolhaas and Dekinga so consistently among taxa that these characters 1993, Hammond and Diamond 1994, Ham- have been used to indicate systematic relation- mond et al. 1994). Detailed studiesof physiology ship (Mitchell 1901, Ziswiler 1967). More ger- and biochemistry of gut function also have dem- mane to ecologistsand functional morphologists onstrated consistent diet-related differences be- is the relationship between the structure of the tween and within species in rates of food pro- digestive tract and diet. This correlation is ap- cessingand nutrient uptake (Karasov and Dia- parent both in measurements of the overall size mond 1983, Levey and Karasov 1989, 1992, of the gut (Leopold 1953, Ziswiler and Famer Martinez de1 Rio and Karasov 1990, Dykstra 1972, Walsberg 1975, Ankney 1977, Pulliainen and Karasov 1992, Obst and Diamond 1992). et al. 1981, Herrera, 1984, Barnes and Thomas The relationship ofgut morphology to diet and 1987, Moss 1989, Richardson and Wooller 1990, food intake suggeststhat the gut is engineered to Karasov 1990) and in the detailed anatomy of match the energetic and nutritional needs of the the walls of the stomach and intestines (Cym- organism without excesscapacity (Hammond et borowski 1968, Brugger 199 1). In addition, size al. 1994). Studies that involve both force-feeding of an individual’s gut may change in responseto (Nir et al. 1978) and experimentally increased food requirements (Hammond and Diamond 1992, 1994) indicate that gut capacity at any giv- en time correspondsclosely to food intake at that I Received2 1 June 1995. Accepted6 February 1996. time. This is consistentwith the principal of sym-

P791 280 R. E. RICKLEFS morphosis (Garland and Huey 1987, Weibel et of the organism, including the composition of al. 199 l), according to which the organism func- the diet. Any correspondencebetween morpho- tions most efficiently when no single component metrics of the digestive tract and ecology of the has a functional capacity in excessof need, or in organism would be consistent with the idea that excess of the functional capacity of any other gut function is costly to the organism and that component. Because gut tissue is expensive to selection promotes matching of gut structure to maintain (Martin and Fuhrman 1955), the size diet, and matching of gut size to food intake. of the gut should be no larger than necessaryto satisfythe nutritional and energeticrequirements METHODS of the organism. Accordingly, one would expect to find a close relationship between the size and FIELD WORK detailed structure of the digestive tract, on one Birds were collected near Rincon de Osa, on the hand, and diet and food requirements, on the Osa Peninsula, southeastern Costa Rica, during other. March 197 1, and near Philadelphia, Pennsyl- Although this relationship has been confirmed vania, during October 197 1. The Costa Rican in a general sense, it has not been investigated samples represented 22 speciesin 11 families or in broadly comparative studies of ecological subfamilies; the Pennsylvanian birds belonged communities or evolutionary to deter- to 12 speciesin nine families or subfamilies. Only mine how resource partitioning within com- one individual was collected per species.Costa munities and evolutionary diversification within Rican birds were captured in mist nets and sac- clades involves the digestive tract. Furthermore, rificed by cervical dislocation. In Pennsylvania, studies with large samples of specieshave been birds were collected by shotgun. Each specimen limited to few measurements of the overall size was weighed to the nearest 0.1 g. The stomach of the gut (e.g., Herrera 1984, 1986, Barnes and was opened to remove its contents, and the stom- Thomas 1987, Wooller et al. 1990) and have not ach and intestines were placed in 10% buffered addressedthe microanatomical structure of the formalin. digestive tract. Microanatomy includes such measurements as the thickness of muscle and glandular layers of the stomach and intestine and GUT DIMENSIONS the absorbtive surface area of the intestine The following external dimensions were mea- (Przystalski 1984, 1985,1986, 1987, 1988),which sured on preserved digestive tracts: length of the undoubtedly have close relationship to gut func- intestine, from the pylorus to the distal end at tion. the junction with the large intestine; the mean In this article, attributes of the structure of the of three measurements of the diameter of the digestive tracts are analyzed for 34 species of intestine (middle of the duodenum, midlength, from Costa Rica and Pennsylvania. and middle of the distal third of the intestine); The purpose of the study was to evaluate the length of the cardiac stomach (gizzard) from the relationship between gut morphology and ecol- junction with the proventriculus to the most dis- ogy. Becausediets of many tropical specieswere tant opposite point; greatestwidth of the cardiac poorly known in 1971 when I collected the ma- stomach roughly perpendicular to the length terials, I had hoped that the diets of birds could measurement. The esophagus, proventriculus, be predicted by the morphology of their digestive caeca, and distal portion of the digestive tract tracts. In the 25 years since the data were ac- (large intestine, rectum) are not considered here. quired, interest in gut function has grown and The caecaof most passerinebirds are small, gen- these data find new contexts in functional mor- erally less than 3% of the length of the small phology and evolutionary diversification. As a intestine (Przystalski 1984, 1985a, 1985b, 1987, consequence,the scope of this study has broad- 1988). Length of the large intestine is approxi- ened. The analyses presented here addressa va- mately 10% of that of the small intestine (Przys- riety of contemporary issues,including (a) scaling talski 1984, 1985, 1986, 1987, 1988). of gut dimensions to body mass, (b) architecture From preserved digestive tracts, the following of the digestive tract as indicated by intercorre- parts were excisedfor imbedding and sectioning: lations among its dimensions, and (c) relation- a central section of the thickest part of the stom- ship of the morphometry of the gut to the ecology ach wall, including the axis perpendicular to the MORPHOMETRY OF DIGESTIVE TRACTS 281 intersection of the length and width measure- dependent contrasts, or PICs (Felsenstein 1985, ments; three 1 cm sectionsof the intestine taken Harvey and Page1 1991, Garland et al. 1992). from points approximately 20, 50, and 80% of PICs were based on the phylogeny of Sibley and the distance between the pylorus and the distal Ahlquist (1990) which included 30 of the species end of the small intestine. Tissue samples were in this study, and they were calculated using the imbedded in paraffin, sectioned at 10 micron CMSINGLE module of the CMAP softwarepro- thickness, mounted on glass slides, and stained gram (Martins and Garland 1991). Included in with hematoxylin-eosin. the analysis were log-transformed values of body An optical micrometer was used to measure mass and the lengths of the stomach and intes- various dimensions of the gut under the micro- tine. The two sets of gastrointestinal PICs were scope.For details of gut anatomy, seeHill (197 1) individually regressedagainst the PICs for body or Ziswiler and Farner (1972). For the stomach, mass, and correlations were calculated among measurements were thicknessesof the muscular the residuals from these regressionsas a check layer at its maximum point, the glandular layer, on the appropriatenessof using phylogenetically and the koilin layer. For the intestine, measure- structured data in this analysis. ments were: overall diameter; thicknessesof the All subsequent analyses were performed on muscular and glandular (mucosal) layers; mean SAS (SAS Institute 1985). To characterize allo- of the lengths of ten villi; number of villi per metric scaling of gut dimensions, body weight cross-section;and diameter of the lumen of the and all dimensions were transformed to common intestine. In addition, total absorptive surface logarithms (base 10) and each of the measure- area of the intestine was calculated as the product ments (X,) was regressed(SAS Procedure GLM) of the total length of the intestine, number of against body mass (M) to determine coefficients villi per crosssection, and doubled length of each of the equation log X, = a, + b,log M, where b, villus. The data set used in subsequent analyses is the allometric constant for measurement i. Re- included the average of the values for each of the siduals (deviations) of observations from the al- three segmentsof the intestine. lometric regressions were retained for subse- quent analyses.Several authors have argued that STATISTICAL ANALYSES bivariate size data should be related by principal Each species was represented by only a single coordinates analysis or major axis regression, specimen in the analysis. Therefore, it was not rather than regression(see LaBarbera [ 19891and possibleto estimate the degreeof variation with- Harvey and Page1[ 199 I] for discussions),how- in speciesor to determine the statistical signifi- ever these techniques produce results that are cance of differencesbetween pairs of species.Co- nearly identical to those of least-squaresregres- efficients of variation (100 x SD/mean) among sion, and so the distinction is not of practical five individuals of each sex of the Great Tit (Pur- importance in this study. Furthermore, residuals US major) averaged 1.5% for the length of the from least-squaresregressions are readily inter- small intestine and 12% for the mucosal surface pretable becausethey portray variation in a sin- area of the small intestine (Przystalski 1986). gle variable rather than a derived axis that is a These values correspond to 0.0065 and 0.052 linear combination of two variables. log,,, units, and are small compared to the range The architecture of the digestive tract was of values observed among speciesin this anal- characterized by correlation (SAS Procedure ysis. Because this study addressesthe relation- CORR) and principal components analysis (SAS ship between gut morphology and other attri- Procedure PRINCOMP) based on the residuals butes of morphology and ecology within a sam- of the log-transformed measurements from their ple of species,each speciesis treated as a datum regressionson the logarithm of body mass. and the total sample size for the analyses that The species included within this study were follow is simply number of species. divided into three diet groups: insects (I), mixed Closely related species may share morpho- insectsand fruits(F), and mixed insectsand seeds metric traits becausethey descendedfrom a com- (S). The diets of the Costa Rican species were mon ancestor; such speciescannot be considered ascertained from Stiles and Skutch (1989); diets as strictly independent samplesof morphological of the temperate species were obtained from variation. The problem of independence can be Martin, Zim, and Nelson (195 1). The gut di- circumvented by calculating phylogenetically in- mensions of these ecological groups were sub- 282 R. E. RICKLEFS

TABLE 1. Speciesincluded in this study,with locationof collection,taxonomic affiliation, and designation accordingto food typeswithin localities*.

Suecies Family Location Diet Body mass(B)

Automolus ochrolaemus Funariidae CR I 141.1 Dendrocinclaanabatina Dendrocolaptidae CR I 42.5 Glyphorhynchusspirurus CR I 13.2 Dendrocolaptescerthia I 65.7 Gymnopithu.?leucapsis2 Formicariidae :: I 29.6 Formicarius analis CR I 61.8 Hylopezus ’ perspicillata I 39.0 Myrmotherulal schisticolor ::: I Schlflornisturdinus Pipridae4 CR F 3;:: Elaenia javogaster Tyrannidae F 23.5 Platyrinchuscoronatus :: I 20.0 Terrenotricuserythrurus CR I 7.5 MionectesoleagineusS CR F 10.8 Tyrannus melancholicus F 39.8 Stelgidopteryxrujicollis Hirundinidae :: 13.3 Parus carolinensis Paridae PA ; 10.1 Parus bicolor PA 21.3 Sitta carolinensis Sittidae PA : 20.9 Microcerculusmarginatus6 CR I 18.8 Mimes polyglottos Mimidae’ PA F 51.9 Turdus grayi Muscicapidae CR F 74.7 Catharus guttatus PA F 31.0 Turdus migratorius PA F 80.0 Reguluscalendula Silviidae* PA I 6.8 Hylophilus ochraceiceps Vireonidae CR I 12.0 solitarius PA F 17.0 Mniotilta varia Parulinae9 PA 10.5 Ramphoceluspasserinii Thraupinae’O 30.3 icterocephala :: 22.0 Thraupis virens CR 34.0 Piranga olivacea PA 31.4 Sporophila aurita Emberizinae” CR 10.4 Melospiza melodia PA 21.2 Pipilo erythropthalamus PA 40.6 * Nomenclaturefrom AOU (I 983) and Sibleyand Monroe (1990). Location:CR = CostaRica, PA = Pennsylvania.Diet: I = insect;F = mixed insectand fruit, S = mixed insectand seed.Food habitsof tropicalspecies from Stilesand Skutch(1989). Nomenclaturalnotes: 1, Sibleyand Monroe (1990) pm thesegenera in the Thanmophilidae;2, Somem e this specieswith G. bicolor of So$ America;,3, Formerly Grallarinperspici/lata; 4> Sibleyand Monrw (1,990)place this speciesm the Fund ~?$yanni~~,Subfamily Tie;&TG Schifformthini;5, FormerlyPipromorpha oleagmea; 6, Species desgnatmnsare not settled(see Stiles ! 983,l 84 ; 7, Mlrnm ofthe Sturm to Sibleyand Monroe (1990); 8, Sylviinaeof the Muwxapidae accordingto AOU (1983); 9, Family Embenz~I~ (AOU 1983), but Tribe Pa@im of the SubfamilyEmberizinae (Fringillidae) according to Sibleyand Monroe (1990); 10, Family Emberizidae(AOU 1983), but Tribe T&iu,puu of the SubfamilyEmberizinae (Fringilhdae) according to Sibleyand Monroe 1990); 11, Family Emberizidae(AOU 1983),but Tnbe Embermm of the SubfamilyEmberizinae (Fringillidae) according to Sibleyand Monroe (196 0). jetted to discriminant analysis (SAS Procedure Monroe (1990). Also included in Table 1 is a CANDTSC), which producesorthogonal, derived simple classification of food resource. A phylo- axes that maximize between-group variance, genetic tree for this sample of species,based on hencediscrimination. Discriminant analyseswere DNA-DNA hybridization estimates of genetic based on the residuals of the log-transformed distance (Sibley et al. 1988, Sibley and Ahlquist measurements from their regressionson the log- 1990), is shown in Figure 1. Two major lineages arithm of body mass. are represented in the data set: (i) the suboscine passerines (Tyrannida) of South American ori- gin, including the antbirds, ovenbirds, and fly- RESULTS catchers,all of which in this sample are tropical, PHYLOGENETIC RELATIONSHIPS WITHIN and (ii) the oscine passerines(Corvida and Pas- THE SAMPLE serida of Sibley and Ahlquist [ 19901).Within the Table 1 lists the speciesincluded in this study , one may recognize as a distinctive with their taxonomic placement by Sibley and group the nine-primaried oscines, including the MORPHOMETRY OF DIGESTIVE TRACTS 283

AT”50(C) 0 insect 0 mixed with fruit 20 15 10 5 0 n mixed with seeds

0 Automolus ochrolaemus l Dendrocincla anabatina l Glyphorhynchus spirurus 0 Dendrocolaptes certhia 0 formicarius analis 0 Hylopezus perspicillatus 0 Gymnopithus leucapsis l Myrmotherula bicolor 0 Mionectes oleagineus 0 Schiifornis turdinus 0 Elaenia ilavogaster 0 Tyrannus melancholicus

l Hylophilus ochraceiceps 0 Vireo solitarius 0 Mimus po/yg/ottos 0 Catharus guttatus 0 Turdus grayi 0 Turdus migratorius l Regulus calendula 0 Stelgidopteryx ruticollis n Parus carolinensis n Parus bicolor n Sitta carolinensis 0 Microcerculus marginatus

n Melospiza melodia 0 Piranga olivacea 0 Thraupis virens 0 Tangara icterocephala 0 Ramphocelus passerinii l Mniotilta varia FIGURE 1. Phylogeneticrelationships of 30 speciesof birds includedin this studybased on the DNA hy- bridization analysisof Sibley and Ahlquist (1990). Four speciescould not be placedin the phylogeny.Three groupsdistinguished by gapsare Tyrannida, Corvida,and Passerida. finches,, and warblers (Fringillidae: Em- pendent contrastsreduced the correlation slight- berizinae). ly, but not significantly. Similar levels of con- cordance between PICs and phylogenetically INDEPENDENT CONTRASTS structured data have been found in other studies Phylogenetically independent contrastscalculat- (Birkhead et al. 1993, Moreno and Carrascal ed for body mass, length of intestine, and length 1993, Ricklefs et al. 1996, Ricklefs and Starck, of stomach suggestthat phylogenetic relation- in press).Estimated allometric slopesusing phy- ships cause little bias in the regressionsand cor- logeneticcontrasts were 0.30 + 0.07 for intestine relations presented in this study. That is, the re- length (F,,*, = 18, P = 0.0003, R2 = 0.40) and sults from the phylogenetically independent con- 0.28 f 0.08 for stomach length (E;,27= 12, P = trasts differ little from results obtained from the 0.0016, R2 = 0.3 1). Again, these slopesare some- original data. For example, among the 30 species what, but not significantly, less than comparable portrayed in the in Figure 1, relationships for the phylogenetically structured the simple correlation between the logarithms of data (0.34 + 0.06 and 0.33 k 0.07, respectively; intestine length and mass was r = 0.7 1. Corre- see Table 2). Residuals of the phylogenetically lations between the phylogenetically indepen- independent contrastswere also significantly cor- dent contrasts for these two variables varied be- related (r = 0.56, F,,Z, = 12.6, P = 0.0014), and tween 0.635 and 0.654 depending on whether the correlation coefficient did not differ signifi- gradual versus punctuated evolution or stan- cantly from that of the similar relationship (r = dardized versus nonstandardized models were 0.46; see Table 4) exhibited by the residuals of chosen. Thus, the use of phylogenetically inde- the original measurements. All subsequentanal- 284 R. E. RICKLEFS

TABLE 2. Allometric (log-log) regressionsof gut measurementson body mass.

Measurement n F P 9 (1 s. b s, RMSE

Intestine 11 Length 34 37.4 0.0001 0.54 0.68 0.08 0.34 0.06 0.101 12 Absorb. surface 43.3 0.000 1 0.62 0.88 0.16 0.72 0.11 0.180 13 Diameter :; 69.5 0.000 1 0.70 0.09 0.05 0.28 0.03 0.062 14 Muscle thickness 31 49.0 0.0001 0.63 0.85 0.14 0.68 0.10 0.177 15 Mucosa thickness 35.4 0.0001 0.56 1.31 0.14 0.59 0.10 0.177 16 Length of villi ;: 8.4 0.0075 0.24 1.54 0.11 0.22 0.08 0.130 17 Number of villi 27 0.1 0.7150 0.01 18 Lumen diameter 31 8.2 0.0078 0.22 1.70 0.13 0.27 0.09 0.170 19 Length of gland 28 11.3 0.0024 0.30 1.32 0.13 0.30 0.09 0.151 110 Width of gland 28 6.1 0.0200 0.19 1.45 0.12 0.22 0.09 0.150 Stomach Sl Muscle thickness 24 0.0068 0.29 -0.09 0.13 0.27 0.09 0.139 S2 Mucosa thickness 24 !:Z 0.0727 0.14 -0.89 0.22 0.29 0.16 0.239 S3 Koilin thickness 20 6.8 0.0180 0.27 -1.09 0.13 0.23 0.09 0.125 S4 Length 33 23.9 0.0001 0.43 0.47 0.10 0.33 0.07 0.122 S5 Width 33 24.3 0.000 1 0.44 0.48 0.08 0.28 0.06 0.103

Note: s,,and sbare the standardemm of the regressioncoefficients a (intercept)and b (slope),respectively. RMSE is the squareroot of the mm mean square,which is similar to the standarddeviation of the residualsabout the regresstonline.

yses use the phylogenetically structured (TIP) portion to the surfacearea of the organism (Mo.67). measurements. The second group of measurements had allo- metric constantsbetween 0.22 and 0.34, and thus ALLOMETRIC RELATIONSHIP TO BODY MASS more closely approximated a “linear dimension” Most gut measurements were strongly allomet- rule (Mo.33).Two gut measurements were not sig- rically related to body mass, M (Table 2, Fig. 2). nificantly related to body mass: number of villi Slopesof the regressionsofthe logarithms ofeach per cross section and thickness of the glandular gut measurement on the logarithm of body mass layer of the stomach. fell into two groups. The first of these, which Przystalski (1984, 1986, 1988) made detailed included absorptive surface area of the intestine measurements of the gut, including length and and thickness of the muscular and glandular lay- surface area of the intestine, on several species ers of the intestine, had values between 0.59 and of passerinebirds (Parus major, Hirundo rustica, 0.72. Thus, thesemeasurements followed a “sur- Regulus regulus, and Erithacus rubecula). As face area” rule, varying approximately in pro- shown in Figure 2, .Przystalski’s measurements

1.6 7 2.4

1.6

I , I I -IL 0.5 1.0 1.5 2.0 0.5 1.0 1.5 2.0 2.5 Log10 body mass (g) FIGURE 2. Logarithmic relationshipsbetween the length and absorptive surfacearea of the intestine and body mass. Regressionsand 95% confidence limits are indicated by the solid and dashed lines. Diet: insect, solid circles; fruit, open circles; seeds,solid squares;species studied by Przystalski, open diamonds. MORPHOMETRY OF DIGESTIVE TRACTS 285

TABLE 3. Allometricrelationships with respectto body massof threemeasures of the digestivetract among 25 speciesof Europeanpasserine birds (datafrom Herrera 1984).

n F P Rl a SE b SE RMSE Gizzard mass(g) 25 124 0.0001 0.844 -1.63 0.13 1.06 0.10 0.152 Intestinelength (mm) 25 139 0.0001 0.858 1.54 0.06 0.53 0.05 0.072 Liver mass(g) 25 160 0.0001 0.875 -1.25 0.08 0.84 0.07 0.105

fall within the range of values obtained in this Thus, compared to tropical species, temperate study, even though calculations of the surface passerinesproduce a higher allometric constant area of the intestine in his studies and in the relating intestine length to body mass in two in- present study differed. Przystalski cut sections dependent samples, but the allometric slopes of tangential to the surface of the intestine to de- other gut measurements do not differ between termine the circumference of the villi and folds temperate and tropical passerines. that projected into the lumen. These circumfer- After the relationship of each gut variable to ences were multiplied by the heights of the villi body mass has been removed by calculating re- and folds as seen in cross-section,and this prod- siduals from allometric regressions,variation in uct was added to the smooth internal area of the a measurement among species is indicated by intestine (at the base of the villi and folds). The variation about the allometric regressionline es- apparent comparability between the measure- timated by the square root of the mean squared ments presented here and those of Przystalski error terms (RMSE). Most of the values in Tables suggestthat calculations of intestinal surfacearea 2 and 3 lie between 0.12 and 0.18 (factors of 1.3 may be estimated reasonably from coarse mea- and 1.5). Somewhat less variable were length surements of surface geometry. (0.10) and diameter (0.06) of the intestine and Herrera (1984) measured lengths of intestines width of the stomach (0.10); somewhat more of 25 speciesof European passerines.The allo- variable was the thickness of the stomach mu- metric relationship of intestine length to body cosa (0.24). mass in his sample (Table 3; b = 0.53 + 0.05) was significantly steeper than that obtained in CORRELATIONS this study (0.34 ? 0.06). To determine whether Correlations among residuals of log,,-trans- this difference might reflect different relation- formed gut measurements portray relationships ships between intestine length and body size for between pairs of these measurements with the tropical and temperate zone species,data from potentially confounding factor of body size re- this study were reanalyzed separatelyfor tropical moved (Table 4). Some of the stronger correla- and temperate taxa. An analysis of covariance tions among residuals were between intestine in which tropical versus temperate was entered length and surface area (Y = 0.49), length of villi as an effectrevealed a significant mass x location (0.56) and length ofthe stomach (0.46); intestine interaction (F,,30= 5.5, P = 0.025), indicating a diameter and length of villi (0.49); thickness of difference in the slopes of the relationships be- koilin and length of stomach (0.67). In Herrera’s tween the two regions. This was confirmed by (1984) study of European passerines, residuals calculating regressionsfor each ofthe groupssep- of length of the intestine were negatively corre- arately. For the tropical sample (F,,,, = 17.4, P lated with residualsof mass of the liver; residuals = 0.0005, R2 = 0.465) the regression was ofboth theseorgans were uncorrelated with those log,,intestine length = 0.747 (f 0.093) + 0.270 of mass of the gizzard (Table 5). (? 0.065) log,,body mass. For the temperate sample (F1,,, = 66, P -c 0.0001, R2= 0.869), the PRINCIPAL COMPONENTS ANALYSIS regression was log,,intestine length = 0.493 (+ Covariation among residuals of gut measure- 0.088) + 0.5 14 (+ 0.063) log,,body mass, which ments may be perceived by means of principal matches Herrera’s result very closely. Similar components analysis. The analysis performed ANCOVAs were run for each of the other gut here was based on a correlation matrix, which measurements, but none of them produced a sig- results in each measurement being normalized nificant mass x location interaction (P > 0.15). by its variation, and thus being given equal weight 286 R. E. RICKLEFS

TABLE 4. Correlationsr, above0.4 amongresiduals of gut measurements.

Variable i Variable j n I P Intestinelength Intestinesurface 28 0.490 0.008 Villus length 28 0.564 0.002 Stomachlength 33 0.461 0.007 Intestinediameter Villus length 28 0.488 0.008 Stomachmuscle 23 -0.47 1 0.023 Villus length Stomachmuscle 20 -0.542 0.014 Stomachmucosa 20 -0.514 0.021 Stomachkoilin Stomachlength 20 0.666 0.001 Stomachlength Stomachwidth 33 0.411 0.018

in the analysis. To produce factor scoresfor each relative size of the stomach is generally inversely species, PCA requires a complete set of mea- related to relative size of intestines in the sample surements. Therefore, to maximize sample size, of speciesincluded in this analysis. only six intestine measurements (I l-16 in Table Insectivorous speciestended to have negative 2) and four stomach measurements (Sl, S2, S4, values, and specieswith mixed diets positive val- S5) were included; these were available for 19 ues, on PC1 (Fig. 3). Species including fruit in species. their diets could be distinguished from those that The first four components had eigenvalues ex- included seedsin their diets on PC2. The only ceeding 1 and togetherexplained 8 1% of the total species conspicuously out of place on this plot variation in the original data (Table 6). The ei- was the tropical, fruit-eating Schzfirnis turdinus, genvalues of these four components were similar which grouped with the insect-eating species. enough that none represent dominant axes of Schzfirnis is the least frugivorous of the man- variation. Loadings on these components none- akins (Stiles and Skutch 1989), and may be more theless show basic patterns in relationships be- properly placed with the flycatchers (Sibley and tween the original variables. The first component Ahlquist 1990). emphasized intestinal measurements (except thickness of mucosa) contrasted with thickness ANOVAS AND DISCRIMINANT ANALYSIS WITH of the stomach wall (muscle and mucosa). The RESPECTTO DIET second component contrasted lengths of the in- Residuals of gut variables were individually sub- testine and stomach with thicknessof the muscle jected to analysesof variance in which diet group layer of the intestine, while the third picked up was the main effect.Four of the ANOVAs showed variation in thicknessof the mucosa of the stom- that gut measurements differed between diet ach and intestine, and the fourth picked up vari- groups, although the levels of significance were ation in the width of the stomach that was con- not high and the effectswere weak (low R2). First, trasted with the thickness of the intestinal mu- stomachswere longer among seed-eaters(0.113) cosa. In general, PCA revealed a negative rela- than fruit-eaters (-0.011) and insect eaters tionship between measurements of size of the (-0.038) (Fz,jo= 7.6, P = 0.03, R2 = 0.21). Sec- stomach and size of the intestine. That is, beyond ond, muscular and glandular layers of the stom- the positive relationships of dimensions of the ach wall were thicker in insect-eaters (0.104, stomach and intestine to body size, variation in 0.189) than in fruit-eaters (-0.094, -0.084) and

TABLE 5. Correlationsamong the residualsfrom allometricregressions on bodymass of measurementsof the digestivesystem of 25 speciesof Europeanpasserine birds (datafrom Herrera 1984).

Correlation with n SD Mill Max Gizzard Intest. Liver Gizzard mass 25 0.149 -0.316 0.395 0.076 0.126 Intestinelength 25 0.071 -0.151 0.146 0.72 0.433 Liver mass 25 0.103 -0.26 1 0.234 0.55 0.03

Note: Correlations are above the diagonal and P-values are below the diagonal. MORPHOMETRY OF DIGESTIVE TRACTS 287

seed-eaters(-0.016, -0.157) (F,,, = 7.6, 7.8; P TABLE 6. Principal componentsanalysis of residuals = 0.003,0.003; RZ= 0.42,0.43). Finally, lengths of 10 gut measurements for 19 species of passerine birds. of intestinal villi were longer in fruit-eaters (0.05 1) and seed-eaters (0.066) than in insect-eaters Measurement PC1 PC2 PC3 PC4 (-0.086) (F2,2s= 5.6, P = 0.01, R* = 0.31). A discriminant analysis including all gut vari- Proportion of ables simultaneously was performed with species variance 0.33 0.21 0.15 0.12 placed in the three diet groups.Like the principal Stomach length 0.38 0.82 -0.06 0.07 Stomach width -0.05 0.15 0.50 0.78 components analysis, the discriminant analysis Stomach muscle -0.65 0.48 0.17 -0.14 was based on a reduced set of variables and in- Stomach mucosa -0.51 -0.25 0.67 -0.01 cluded only 19 speciesfor which these data were Intestine length 0.71 0.59 0.13 -0.04 complete. Intestine diameter 0.78 -0.41 0.09 -0.04 Two discriminant axes separated the groups Surface area 0.60 0.30 0.55 -0.09 Intestine muscle 0.51 -0.73 0.33 0.11 unambiguously (Table 7), reinforcing the results Intestine mucosa -0.03 0.18 0.50 -0.70 obtained in the individual ANOVAs. Indeed, in- Villus length 0.84 -0.02 -0.17 0.16 sect-eaters were separated from species with V&U% are the correlations of each independent variable with each mixed diets by a large gap in morphometric space principal component. (Fig. 4). The insect group was distinguished from the others on the first discriminant axis by having small, but thick-walled stomachs,and relatively case was there significant discrimination of the small (length and diameter) intestines, but per- groups (Fw., = 0.83, P = 0.66, and F,2,44= 0.68, haps with thick mucosae. Speciesthat included P = 0.76, respectively). fruit in their diets were less clearly distinguished To determine whether phylogenetic relation- from those that included seeds by the second ship is associated with degree of resemblance discriminant axis. The highestvalues on this axis among measurements of the digestive tract, I (thick intestinal mucosa and muscle layer, rela- conducted discriminant analyses in which the tively short stomachs) belonged to fruit-eaters, groups were the three parvorders Tyrannida, and the lowest values belonged to seed-eaters. Corvida, and Passerida. The first analysis, in- A seconddiscriminant analysis was performed cluding 19 species, did not produce significant with a reduced number of gut variables in discrimination (Wilk’s lambda, F2,,14= 1.5, P = to increase the sample of species included. By 0.2) but suggestedthat members of the Tyran- dropping thickness of the stomach wall, and length of villi, and absorbtive surface of the in- testine, the sample was increased from 19 to 30 species.This discriminant analysis (Table 7) re- vealed patterns similar to the first. Insect-eaters had small stomachsand short intestines,but thick intestinal mucosae, compared to the others. On the second discriminant axis, fruit-eaters were distinguished from the other speciesby having thick intestines with thick muscle layers. The poorer discrimination of the insect-eaters from specieswith mixed diets in this analysis appar- ently resulted from deleting thicknessof the mus- -2 cular and mucosal layers of the stomach as vari- ables, as these were important in distinguishing -3 the groups in the first analysis. -4 -3 -2 -1 0 1 2 3 To confirm that the discriminant analyseshad PCA axis1 biological meaning, I randomly assignedspecies to three groups with equal probability and ap- FIGURE 3. Distribution of 19 species of on principal components (PC) axes 2 and 3 based based plied discriminant analysesto thesegroups based on a correlation matrix of the residuals of log-trans- on the sets of characters for which the sample formed values of gut measurements.Diet: insect, solid was 19 and 30 species, respectively. In neither circles; fruit, open circles; seeds,solid squares. 288 R. E. RICKLEFS

TABLE 7. Canonical discriminant function analysisbased on residualsof 10 gut measurementson 19 species, or on 6 gut measurementsof 30 species,of passerinebirds.

19 Species 30 species CAN1 CAN2 CAN1 CAN2

Statistics Eigenvalue 18.4 0.8 0.92 0.69 Canonical correlation 0.97 0.67 0.69 0.64 F 3.5 0.7 2.9 3.2 Numerator degreesof freedom 20 9 12 5 Denominator degreesof freedom 14 8 44 23 P 0.01 0.68 0.0045 0.026 Canonical structure Intestine length 0.99 0.01 0.94 0.34 Intestine diameter 0.89 0.46 0.10 0.99 Intestine surface 0.98 0.21 Intestine muscle 0.68 0.74 0.44 0.90 Intestinemucosa -0.80 0.60 -0.96 0.27 Villus length 0.99 0.09 Stomachlength 0.74 -0.67 0.91 -0.42 Stomachwidth 0.97 0.24 0.81 -0.58 Stomachmuscle -0.93 -0.37 Stomachmucosa -0.96 0.28 Group means Insectdiet (n = 7) -5.12 -0.13 -0.84 -0.63 Mixed insectand fruit (n = 7) 2.50 0.95 0.01 0.96 Mixed insectand seed(n = 5) 3.67 -1.16 1.65 -0.66 nida have comparatively thick-walled, wide ple, all the seed-eatersin this sample belong to stomachsand small (length, width) intestines. A the Corvida and Passerida,while few of the em- larger sample with fewer variables provided a berizids have purely insect diets. Among the Tyr- similar picture with significant discrimination annida, insect-eaters and fruit-eaters separate (F,,,d, = 2.3, P = 0.02). The variables that dis- largely along phylogenetic lines. Therefore, we tinguish the Tyrannida from other taxa are the may ask whether specieswithin each of the diet same variables that distinguished insect-eating groups exhibit similar morphology because of species from those with mixed diets. For both common ancestry or becausethey have respond- the larger and smaller set of variables, however, ed to similar selective factors. diet provides better discrimination among spe- The discriminant analysis depicted in Figure cies than does . 4 places speciesin diet groups together in mor- phological space,regardless of the ancestry of its DISCUSSION members. Insect-eaters and fruit-eating mem- bers of the Tyrannida are clearly distinguished PHYLOGENETIC CONSIDERATIONS from each other, and each allies with speciesof Although speciesincluded in this analysis exhibit the Corvida and Passeridain the samediet groups. varying degreesof relationship, analysis of phy- Discriminant analysis gives better discrimina- logenetically independent contrastsindicates that tion when groups are based on diet rather than correlations between gut measurementsand body taxonomy. size, or among gut measurements, are not strong- ly influenced by the phylogenetic structure of the SCALING OF GUT DIMENSIONS data sets. For statistical purposes, each species Gut dimensions included in this study relate to can be considered as an independent data point. several important features of the digestive tract, A separate phylogenetic issue is whether cer- including volumes of the stomach and intestine, tain combinations of ecology and morphology relative strengthsof muscles that grind and mix are restricted to certain parts of the avian phy- food in the stomachand move the digestathrough logeny included within this data set. For exam- the intestines, secretory capacity of gastric and MORPHOMETRY OF DIGESTIVE TRACTS 289

-2

-3 -8 -6 -4 -2 0 2 4 6 -4 -2 0 2 4

Discriminant axis 1 Discriminant axis 1 FIGURE 4. Left: Distribution of 19 speciesof bird on discriminant function axes 1 and 2 based on grouping speciesinto diets consistingof: insect, solid circles; fruit, open circles; seeds,solid squares.Right: Distribution dased on 30 speciesusing fewer gut variables. intestinal mucosae, and absorbtive surface area time, the average period required by undigested of the intestine. This analysis indicates that these material to pass through the digestive tract, is dimensions bear certain relationships to each equal to length of the gut divided by rate of pas- other and to aspectsof the ecological relation- sage.Taking the allometric constants of L and S ships of species,which presumably are expressed to be 0.34 and 0.16, respectively, I can estimate in diet and food intake. These results are con- that retention time should scaleto the 0.18 power sistent with the idea that the gut respondsto the of body mass, which is close to the empirical kind and amount of food it receives according value of 0.21 determined over a wide range of to certain optimal design principles. speciesby Karasov (1990). Allometric analysesshow that most of the lin- Three gut dimensions had allometric constants ear dimensions of the gut scale as the approxi- closer to the Y3 power of body mass: absorbtive mately % power of body mass, which is consis- area of the intestine and thickness of muscle and tent with proportional scaling of linear dimen- mucosal layers of the intestine. If we assumethat sions (McLelland 1979). In fact, several dimen- circumference of the intestine, like its diameter, sions have allometric constants somewhat less is proportional to the L/3 power of body mass, than 0.33, suggestingthat the gut becomes rel- then both muscular and mucosal cross-sectional atively smaller in larger birds. Total volume of areas of the intestine should vary in direct pro- the intestine is length times cross-sectionalarea; portion to body mass. The cross-sectionalarea the latter is proportional to the square of the of the intestine varies as the *I3 power of mass, diameter. Because length (L) and diameter (0) suggestingthat increasing intestinal diameter re- had allometric constants of 0.34 and 0.28 in this quires a proportionately greater increase in in- study, the allometric constant of volume (LD) testinal tissue mass. would be 0.90, that is, slightly (but not signifi- It is intriguing that the absorbtive surface of cantly) less than proportional to body weight. the intestine scalesabout the same (0.72) as The rate of passageof material through the in- metabolic rate (0.72; Calder 1985) and maxi- testine (or speed,S, distance time-l) should scale mum daily metabolizable energy (0.72; Kirk- approximately as the volume of contents digest- wood 1983) scale among passerine birds. This ed per unit time divided by the intestinal volume suggeststhat surface area is the basic variable and multiplied by the length of the gut. If we that birds manipulate to increaseor decreasetheir assume that the volume digested per unit time capacity to assimilate energy or nutrients. Al- is proportional to metabolism (allometric con- though rate of absorbtion per unit of intestinal stant, 0.72; Calder 1984) then rate of passage surface may vary considerably among species along the gut should scale as the 0.72 (volume (Karasov and Levey 1990) it does not appear to time-‘) - 0.90 (volume) + 0.34 (length) = 0.16 be a major component of variation among spe- (length time-‘) power of body mass. Retention cies with respectto body size. It would be inter- 290 R. E. RICKLEFS

esting to determine the relationship between the GUT MORPHOMETRY AND ECOLOGY surface area of the gut and the daily energy ex- Pure insectivores differ from birds with mixed penditure on a species-for-speciesbasis. diets in having short intestinesand villi and thick- If intestinal surface area were matched to en- walled stomachs. This suggeststhat much of the ergy or nutrient requirement, one would expect work accomplished by the guts of insectivores a general correlation between rate of metabolism occurs during the grinding of food (hard-bodied and relative size of the gut surfaceamong species insects) and digestion in the stomach, perhaps of similar body size. If such a correlation exists, largely through hydrolysis of proteins, and that it would be revealed by residuals about the al- further processingof the digesta and its absorb- lometric regressionof intestinal surfacewith body tion are a relatively smaller part of the overall mass. Half of the 28 speciesincluded in this re- digestive process.All other speciesinclude fruits gression (Table 2) had residuals greater than and seedsin their diets to varying degrees.Seed- +O. 15 or less than -0.15. The lowest quartile eaters do not have heavy grinding stomachstyp- of values belonged mostly to tropical taxa: Hy- ical of doves and galliforms, perhaps because lophilus (-0.38), Thraupus (-0.29, Tangara speciesincluded in this sample husk seedsbefore (-0.25), Automolus (-0.23), Platyrynchus swallowing them. The relatively larger intestines (-0.20), and Turdus grayi (-0.16), along with of fruit- and seed-eaters may reflect the larger the temperate resident Regulus (-0.16), and in- proportion of carbohydratesin the diet. The thick cluded both insect-eating and fruit-eating spe- muscle and mucosal layers of the intestines of cies. The highest values belonged to two neo- fruit-eaters may be related to the large volume tropical migrants: Piranga (+0.27) and Stelgi- and high water content of the diet. dopteryx(+0.25); two partial migrants: Catharus Clearly, the structure of the gut is related to (+0.26) and Melospiza (+0.20); and two tropical diet. The resultsof this and related studiesshould species: Elaenia (+ 0.19) and Dendrocinchla be extended by additional comparative mea- (+O. 16). None of the variation in absortive sur- surements, including fine-scale anatomy. To in- face makes apparent sense in terms of ecology terpret anatomy properly, however, studies re- or diet; data on daily metabolic rates are not lating gut function and anatomy also should be available for these species. pursued. Finally, a better understanding of the GUT ARCHITECTURE biochemical composition and structural qualities of different foods would provide needed detail The intestinal absorbtive surface is the product of the diet-gut relationship and allow us to un- of intestine length, villus length, and number of derstand functional constraints on diet selection villi per cross-section.In this study, villus num- and evolutionary modification of the gut. ber exhibited little variation among speciesand was not significantly related to body mass. Ac- cordingly, intestinal surface area was strongly ACKNOWLEDGMENTS correlated with length of intestine (r = 0.79) and I am gratefulto SusanProgoff and SharonWeremiuk length of villi (r = 0.61), but not with number for assistancein the laboratory.The microscopywas of villi per crosssection (r = 0.32). supportedby a grantfrom the National ScienceFoun- Another important feature of gut architecture dation.Analysis and thewriting was supported by NSF BSR9007000.D. J. Levey, J. M. Starck,J. Sedinger, among passerine species was the inverse rela- and an anonymousreviewer provided valuable com- tionship between measurements of thickness of mentsand discussion. the stomach wall and several measurements of the intestine, particularly length of villi and di- LITERATURE CITED ameter of the intestine. Thick stomach muscles (and mucosae) are found primarily among trop- AMERICAN ORNITHOLOGISTS ’ UNION. 1983. Check- list of North American birds. 6th ed. American ical species,particularly insectivores. Discrimi- OrnithologistsUnion,’ Washington,DC. nant function analysis also revealed that these AL-DABBAGH, K. Y., J. H. JIAD, AM) I. N. WAHEED. specieshave thick gastric and intestinal mucosae 1987. The influenceofdiet on theintestine length and short villi. One is tempted to explain this of the White-cheekedBulbul. Omis Scan.18: 150- pattern by relating thick gastricmuscles and both 152. ANKNEY,C. D. 1977. Feedingand digestiveorgan gastic and intestinal mucosae to more complete sizein LesserSnow Geese. Auk 94:275-282. digestion, thereby reducing requirements for di- ANKNEY,C. D., ANDS. M. Scorr. 1988. Size of di- gestion in the intestine. gestive organs in breeding Brown-headed Cow- MORPHOMETRY OF DIGESTIVE TRACTS 291

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