Digestive responses to changes in diet, season, photoperiod, and temperature by the red-winged blackbird (Agelaius phoen...


Material Information

Digestive responses to changes in diet, season, photoperiod, and temperature by the red-winged blackbird (Agelaius phoeniceus)
Physical Description:
vii, 105 leaves : ill. ; 29 cm.
Brugger, Kristin E., 1955-
Publication Date:


bibliography   ( marcgt )
theses   ( marcgt )
non-fiction   ( marcgt )


Thesis (Ph. D.)--University of Florida, 1989.
Includes bibliographical references (leaves 96-104).
Statement of Responsibility:
by Kristin E. Brugger.
General Note:
General Note:

Record Information

Source Institution:
University of Florida
Rights Management:
All applicable rights reserved by the source institution and holding location.
Resource Identifier:
aleph - 001563054
notis - AHH6780
oclc - 22711623
System ID:

Full Text








I thank members of my supervisory committee for their support and

encouragement throughout my years of graduate study. M. W. Collopy

supervised and shepherded the project to completion. K. A. Bjorndal

provided training in techniques of nutritional analyses, access to

laboratory facilities, and carefully criticized the work. D. J. Levey

introduced me to problems in nutritional ecology of birds and also

actively criticized the dissertation. R. A. Kiltie, J. G. Robinson,

and G. W. Tanner offered advice and straight thinking.

Several others contributed to the work. C. Martinez del Rio,

Department of Zoology, assisted in the diet switch experiment. G.

Foster, Biologist, supervised lab analyses and prepared solutions. J.

E. Moore, Department of Animal Sciences, and R. D. Miles, Department of

Poultry Sciences, improved my understanding of animal nutrition.

The dissertation was supported as part of a research contract and

Cooperative Education Agreement between the U. S. Fish and Wildlife

Service (USFWS) and the University of Florida, Department of Wildlife

and Range Sciences. I thank N. R. Holler (USFWS, Cooperative Fish and

Wildlife Research Unit, Auburn University, Auburn, Alabama) and H. F.

Percival (USFWS, Cooperative Fish and Wildlife Research Unit,

University of Florida, Gainesville, Florida) for developing the

projects and for continued encouragement and advice during the program.

I thank R. F. Labisky for administering the contract and for his

contributions to the dissertation research.

The Denver Wildlife Research Center (DWRC), formerly of the U. S.

Department of Interior, now of U. S. Department of Agriculture, Animal

and Plant Health Inspection Service (USDA/APHIS), provided tremendous

logistical and financial support to carry out feeding trials. The work

could not have been accomplished without the assistance of M. L. Avery,

Project Leader, Florida Field Station, who provided research

facilities. R. A. Dolbeer, Ohio Field Station, was helpful in advising

during the early stages of the program. I thank C. O. Nelms and D. E.

Daneke for assistance in the lab.

Technical assistance was provided by J. M. Matter for histological

preparations, by P. T. Andreadis for blood sampling techniques, and by

P. Scheerin for testosterone assays. Computer facilities and office

space were provided during the period of writing the dissertation by M.

L. Crump and P. Feinsinger.

Throughout it all, H. M. Tiebout III offered sage advice,

patience, love and unwavering support. I am grateful to Harry for



ACKNOWLEDGMENTS............................................... ii

ABSTRACT................................................. .... vi

INTRODUCTION.................................................. 1

BACKGROUND.................................................... 6

Theories of Digestion.. ................................ 6

Digestive Strategy................................. 6
Optimality Models.................................. 8
Empirical Models................................... 12
Synthesis........................................ .15

Red-Winged Blackbirds: Diet Generalists................. 16

Food Habits........................................ 16
Anatomy of the Gastrointestinal Tract............. 17
Energetics....................................... .19

METHODS....................................................... 21

Overview................................................. 21

General Procedures...................................... 22

Collections. ..................................... 22
Housing........................................... 23
Digestion Trials................................... 23

Study Design............................................ 25

Experiment I: Diet Quality........................ 25
Experiment II: Season.............................. 29
Experiment III: Photoperiod...................... 29
Experiment IV: Temperature....................... 30

Measurements and Analyses............................... 30

Retention Time..................................... 30
Gut Anatomy....................................... .32
Food Assimilation................................ 33
Data Analyses. ..................................... 36

RESULTS .................... ................................. 41

Experiment I: Diet Quality ..... ......................... 41

Nitrogen Balance and Body Mass.................... 41
Intake, Defecation, and Metabolizable Energy
Intake........................................... 47
Digestibilities................................... 52
Gut Anatomy....................................... .56

Experiment II: Season................................... 61

Intake, Defecation, Metabolizable Energy Intake,
and Transit.................................... 61
Digestibilities................................... 65
Gut Anatomy....................................... .67

Experiment III: Photoperiod............................. 67

Intake, Defecation, Metabolizable Energy Intake,
and Transit.................................. 68
Digestibilities...................... ............. 68
Body Mass, Gut Anatomy, and Reproductive
Condition........................................ 68

Experiment IV: Temperature ............................... 70

Intake, Defecation, Metabolizable Energy,
and Transit.................................. 70
Digestibilities................................... 72
Body Mass and Gut Anatomy......................... 72

DISCUSSION.................................................... 74

Intake and Digestibilities.............................. .74

Exogenous Factors.................................. 76
Endogenous Factors................................. 82
Fiber Digestion ................................... 82

Morphological Responses................................ 84

Exogenous Factors.................................. 84
Endogenous Factors................................. 87

Predictions of Digestion Theory......................... 88

Gut Capacity...................................... .88
Retention Time..................................... 91
Hydrolysis and Absorption ......................... 93

Summary and Conclusions................................ 94

LITERATURE CITED............................................. 96

BIOGRAPHICAL SKETCH............................................. 105


Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy



Kristin E. Brugger

December 1989

Chairman: Michael W. Collopy
Major Department: Forest Resources and Conservation
(Wildlife and Range Sciences)

Four feeding experiments were conducted to identify digestive

responses (intake, digestibilities, gut anatomy, retention) by Red-

winged Blackbirds to changes in diet, season, photoperiod, and

temperature. In a 40-d experiment, 3 diets that varied up to 15% in

energy contents were tested. Intake varied 30%. Metabolizable energy

coefficients (MEC) varied 15%, nitrogen digestibility 25%, and fiber

digestibility 30%. Gizzard mass varied 17%, small intestine length

(SIL) 9%, and villus length 17%. Digestibilities were not related to

intake or SIL. Volumetric intake and SIL were directly related. No

measures of retention were obtained.

In a 1-yr feeding experiment, response to seasonally fluctuating

demand was tested using a single, controlled diet. Intake was highest

in winter. The MEC/intake slope was positive in autumn and winter, but

0 in spring and summer. One gut organ varied among seasons: large

intestine length was 28% larger in summer than winter. Intake and SIL

were not related. Retention, estimated by transit, did not vary among


In a 30-d experiment with 2 photoperiod treatments, daylength had

no effect on intake, digestibilities, gut anatomy, or transit. In a 30-

d experiment with 2 temperature treatments, intake was 30% greater and

gizzard mass 24% greater in birds at 7 oC than 20 OC. Birds at 7 OC

assimilated 10% more energy/d than those at 20 OC, but did so 10% less

efficiently. Digestibility of organic matter was 10%, nitrogen 30%, and

fiber 25% less in birds at 7 C than 20 OC. Transit did not differ

between treatments.

Data were used to evaluate 3 predictions of digestion theory: (1)

if intake is fixed and demand increases, retention time should increase;

(2) if gut capacity is not flexible and demand increases, absorption

should increase; and (3) if diet quality decreases and metabolic demand

remains the same, gut capacity should increase. The third prediction

was supported. Diet quality, in the range offered, elicited the

greatest ranges of digestive responses, when compared with those of the

other tests. Behavioral flexibility in food choice and intake thus may

determine the range of potential digestive responses in Red-winged



Red-winged Blackbirds (Agelaius phoeniceus) have undergone a rapid

increase in population size in North America since 1950 (Dolbeer and

Stehn 1979). This population growth is attributed to large-scale

conversion of land to agricultural uses since World War II (Graber and

Graber 1963), coupled with the generalist feeding habits (Beal 1900)

and unusually high reproductive potential (Stehn 1989) of the birds.

For example, in Quebec, the 200% increase in population density of

breeding redwings between 1966 and 1981 is attributed not only to

increased availability of food in the southwestern grain production

regions, but also to increased habitat availability and flexibility in

food choice by adults (Clarke et al. 1986, McNicol et al. 1982).

Flexibility in food resource use may be key to the successful expansion

of populations with very high reproductive potential.

The digestive abilities of an animal may influence food choice and

therefore resource use (Martinez del Rio et al. 1988, 1989), thus

serving as a link between the food base and productive capacity.

Feeding and breeding habits of redwings are well known (Crase and

DeHaven 1975, Stehn 1989). However, little is known of the abilities

of redwings to digest the variety of foods encountered during their

daily and seasonal shifts in diet (Hintz and Dyer 1970). My research

addressed the question of what features of the digestive system enable

redwings to process a broad diet throughout the year.

Digestive abilities might change as a result of short-term

adaptation by the gastrointestinal tract. Several models for digestion

(Milton 1981, Penry and Jumars 1986, 1987), digestion and absorption

(Sibly 1981, Moss 1983, Karasov 1987, in press), and short-term

morphological adaptation by the gastrointestinal tract (Robinson et al.

1981) have been posed. The gut may adapt to variation in factors such

as food composition, daylength, temperature, metabolic demands, or

physiological status (e.g., breeding and molt). Responses by the gut

to accommodate changing intake or to promote variable nutrient uptake

might include alteration of (1) size, (2) retention time, (3) pre-

absorptive processes, or (4) absorption rates. Cumulative effects or

interactions of these responses could significantly affect net gain of

energy or nutrients, thus improving the ability of an animal to

maintain nutrient balance.

Birds show several digestive responses to variation in their

external environment. Seasonal variation in sizes of gastrointestinal

organs within populations of wild birds is well documented. Birds in

the orders Anseriformes (Miller 1975), Galliformes (Moss 1974),

Columbiformes (Kenward and Sibly 1977), and Passeriformes (Al-Joborae

1980) show such patterns. Small intestine and ceca are longest during

winter when food quality is low and metabolic demand is high.

Intestinal growth can be elicited by manipulating diet in laboratory

experiments, suggesting dynamic response of the gut (Savory and Gentle

1976a 1976b, Al-Joborae 1980). Alteration of pre-absorptive processes

may occur with facultative induction of enzymes or increase in

transport also as a response to diet, but little information is

available (Karasov and Diamond 1987).

Birds show seasonal change in food selection and assimilation,

presumably as a response to endogenous metabolic demands. Captive

Garden Warblers (Sylvia borin) in the absence of external cues changed

monthly intake of fruits relative to insects (Berthold 1976). Captive

American Robins (Turdus migratorius), exposed to natural photoperiod

and controlled temperature, also demonstrated circannual changes in

fruit consumption (Wheelwright 1988). Seasonal.increases in

efficiencies of food assimilation were demonstrated in Garden Warblers

and were attributed to mechanisms associated with premigratory

fattening in these long-distance migrants (Bairlein 1985). To date,

there are no experimental data that partition the relative effects of

diet, season, photoperiod or temperature on digestive performance in

wild birds.

Red-winged Blackbirds provide a model for examining digestive

responses. They have a generalist diet, simple digestive anatomy, and

marked seasonal fluctuations in food type, physiological status, and

metabolic demands. Thus, redwings are likely candidates to exhibit

digestive processes that might respond to change in diet, season,

photoperiod, or temperature. I had 2 primary objectives for this


(1) to quantify the variability in digestive performance and gut

anatomy associated with changes in diet, season, photoperiod,

and temperature;

(2) to apply these data to predictions of digestion theory (see

pp. 6-16)

(a) if intake is fixed and metabolic demand increases,

retention time should increase,

(b) if gut capacity is not flexible and demand increases,

hydrolysis and absorption should increase, and

(c) if diet quality decreases and metabolic demand and

intake remain the same, both retention time and gut

capacity should increase.

Two secondary objectives were identified as the research

proceeded. Adaptations to diet may occur in intestinal villi of birds,

as has been identified in mammals. For example, the villi of

laboratory rats change in length in response to nutrients in the

intestinal lumen (Johnson 1987). The net effect of increased villus

length is increased surface area for absorption. Thus an additional

objective of study was

(3) to determine if villus length varies in redwings when they

are fed different diets.

Sex hormones may affect gastrointestinal growth, thus affecting

digestion. Increased blood concentrations of testosterone result in

growth of length and thickness of the small intestine in mice (Wright

et al. 1972). The opposite was found in birds. High testosterone

concentration was correlated with depressed growth of skeletal muscle

(Scanes 1987). Thus, the final objective for study was


(4) to determine if a relationship exists between reproductive

condition, as measured by testosterone concentration in the

blood, and sizes of gastrointestinal organs or measures of

digestive performance in the male redwings that were tested in

these feeding experiments.


Theories of Digestion

Digestion is but one of five stages in the general process of

animal nutrition, which include foraging, digestion, absorption,

circulatory transport, and metabolism. Many theories of foraging have

been presented (Stephens and Krebs 1986), and they rely primarily on

the procedures of optimization modelling to develop an understanding of

food choice by animals. A similar approach has been used in the

development of theories of digestion. However, these theories often do

not separate the related processes of digestion (e.g., hydrolysis) and

absorption (e.g., uptake across the intestinal wall), leading to some

lack of clarity. Additionally, several empirical models have been

presented that provide a practical perspective on the limits of

combined digestive and absorptive responses. Below I review these

theories and summarize their predictions with respect to the responses

that might be observed in the Red-winged Blackbird.

Digestive Strategy

The concept of a digestive strategy was posed to explain food

choice by African ungulates and serves as a useful framework for

understanding the range of digestive responses possible by animals

(Bell 1971, Milton 1981). Digestive strategies are formed by the

relationship of the efficiency of nutrient extraction in the gut, with

efficiency defined as total extraction for a given meal, and the

velocity of food passage. The 2 variables interact to determine food

chioce and diet specialization.

An efficiency-velocity continuum was presented, along which

animals could be placed depending on whether their digestive strategy

is to maximize digestive efficiency or to maximize velocity of food

passage (Bell 1971, Milton 1981). For example, an animal with a

voluminous digestive tract should be able to extract more energy or

nutrients from a given meal because food remains in the system longer

than in one with a small digestive tract. Therefore it could

specialize on fibrous or energy-dilute foods. The animal with a large

digestive tract would be positioned at the opposite end of the

continuum than one with a small tract. The efficiency-velocity

continuum thus represents interspecific variation in the range of

digestive constraints to food selection. Milton (1981) predicted that,

once a digestive strategy has evolved, there is little possibility for

switching among diets by an animal.

In contrast to Milton's prediction, omnivores and seasonal diet

shifters regularly switch among diets. The concept of a digestive

strategy, therefore provides a framework for predicting digestive

responses to changing diets within a species. As individual birds

undergo seasonal diet shifts and choose foods that differ in energy

densities or ease of energy extraction, there should be a seasonal

shifting along the efficiency-velocity continuum. Therefore, velocity

should slow seasonally, resulting in greater efficiency, or extent of

nutrient extraction.

Optimality Models

Optimization modelling (Bellman 1957) has proven useful to

foraging theory by developing predictive models, and has been applied

to digestion. As with foraging theory, digestion theory is based on

the premise that survival or reproductive success depends on the rate

at which energy is obtained. Therefore, the objective of the

optimization problem is to maximize net rate of energy gain by


Optimal digestion. A theory of optimal digestion, with implicit

references to absorption, was posed by Sibly (1981) for monogastric

animals with continuous flow digestive systems. He focused on bird

digestion and created a simple time-energy model of digestive

performance, with three phases of energy cost-benefits: (1) an energy

cost associated with cracking the food's defenses and digesting large

molecules; (2) a rapidly increasing energy benefit during early

digestion and absorption; and (3) a declining energy benefit during

digestion and absorption of the last bits of material in the gut. The

resulting curve is described by a function, f(T) (Fig. 1). The model

can be reformulated in terms of maximizing the intake of important or

limiting nutrients.

Sibly (1981) reasoned that the net rate of obtaining energy from

food in the digestive tract is a function of (1) the rate of ingestion

Phase 1 Phase 2 Phase 3


5 y ....-- g(T)

I" / /


I *I

Retention Time

Figure 1. Sibly's (1981) time-energy model of digestion, described by
the function, f(T). In the first phase, the energetic cost
of cracking the food's defense systems and breaking
molecular bonds results in a net energy loss. In the
second phase, a rapidly increasing energy gain is
associated with absorption of easily digested foods. In
the third phase, a declining rate of energy gain is
observed as the last bits of food are digested. The slopes
of lines at 2 points on the curve, described by f(T)/T,
represent 2 volumetric processing rates (per unit retention
time). A diet with lower energy content would necessarily
have a lower set of energy gain values, shown here as g(T).

of foods (r), (2) the retention time of food in the digestive tract

(T), and (3) the time-energy function for food processing, f(T),

described by the equation

Net rate of obtaining energy = r f(T). (1)

For a bird, the energetic cost of flight depends upon body mass. Thus,

the mass of the digestive tract, including organs and digesta, should

affect optimization. The mass of digesta carried per unit time by a

bird is equal to the rate of ingestion (r) multiplied by the retention

time (T). Substituting for r (r = mass carried/T) gives the equation

Net rate of obtaining energy = mass carried f(T). (2)

Substituting further, the value (f(T))/T is derived. It is interpreted

as the volumetric processing rate per unit of retention time, which

measures how well a given meal can be digested and absorbed in a

specific amount of time. It is represented by the slope of the line

that extends from the origin to a point on the curve f(T) that

corresponds with the specific retention time T.

Three predictions of how animals should meet decreases in food

quality or increases in nutrient demand emerged from Sibly's (1981)

theory of optimal digestion. (1) When intake is fixed and metabolic

demand increases, an animal should increase retention time (T) to

increase the extent of energy gain. Thus if intake is limiting,

digesta should remain in the gut longer than when intake is not

limited. (2) When metabolic demand increases, if the digestive tract

is limited in size, then for a given weight of digesta carried by an

animal, the optimal strategy is to increase (f(T))/T, or the rate of

obtaining energy by digestion per unit retention time. Thus if the

capacity of the gut cannot be increased to hold more food when demand

increases, then the rates of physical and chemical breakdown and rates

of absorption should be increased. This will permit an increased rate

of food intake. (3) The size of the digestive tract should be larger

when an animal is eating a poor-quality diet than when it is on a high-

quality diet, assuming metabolic demand remains the same between diets.

Thus there should be short-term growth of the gut to hold more food

during the time of year when diet is poor. This is because the food

processing curve, f(T), has a lower set of energy-gain values for a

poor-quality diet than for a high-quality diet (Fig. 1). It follows

that the maximum value of (f(T))/T for a low-quality diet is lower than

that for a high-quality diet.

Chemical reactor analysis. Penry and Jumars (1986, 1987) created

a general theory of optimal digestion using the operating policies and

optimization constraints of principles of chemical-reactor theory

(Levenspiel 1972). Three industrial reactor systems that lend

themselves to mathematical modelling were viewed as approximations of

animal digestive systems--batch, plug-flow, and continuous-flow

stirred-tank reactors (CSTR).

In summary from Penry and Jumars (1986), a batch reactor works in

complete cycles of ingestion, digestion, and egestion, such that it

takes in all reactants at once, reactants are mixed thoroughly and

allowed to react, then all materials are completely removed from the

reactor. Animals modeled as having batch-reactor guts include hydras,

jellyfish, sea anemones, and starfish. Plug-flow reactors have a

continuous, orderly flow of material from entrance to exit. Material

is perfectly mixed radially; mixing between plugs along the length of

the flow path does not occur. Animals with guts that approximate plug-

flow reactors include birds and deposit-feeding polychaetes with simple

tubular guts. Reactors with continuous-flow, stirred-tanks incorporate

both constant flow of material through the reactor and complete mixing

within it. No animal perfectly fits the CSTR model, but ruminants

operate a portion of the gut as CSTR, and another portion as plug-flow.

Reactor-specific mass-balance equations for chemical reactions

were used to identify how animals with batch, plug-flow, or CSTR guts

might respond to changes in diet or metabolic demands. In each case,

for a given reaction rate, the ratio of gut volume (u) to volumetric

flow rate (Vo) emerged as the most important variable (U/Vo =

throughput time). Maximizing energy production rates calls for

minimizing the throughput time required for a given reaction. Penry

and Jumars (1986) concluded that, for each gut type, volume should be

varied whenever the composition of an animal's diet changes, thus

promoting variable retention and allowing the animal to maintain

constant efficiencies of energy or nutrient use while exploiting diets

of diverse qualities.

Empirical Models

Morphology. absorption. and intake. Moss (1983) presented a model

of digestion for ptarmigan (Lagopus spp.) and grouse (Lagopu, Tetrao,

and Canachites spp.) that related the average digestibility of foods

(D) to surface area of the gut (A), absorption rate (k), and food

intake (I)

D a (k A)/I. (3)

Moss (1983) reasoned that the value of k depended partly on the nature

of the food and partly on the length of time the food spends in the

gut. Retention time is inversely related to food intake for a given

gut; therefore the digestibility of the food varies inversely with I.

Moss (1983) found in ptarmigan and grouse that surface area of the gut

is related to body weight and gut length, and substituted those values

for A. He concluded that the observed digestibility of a food type

depended partly on the physiological abilities of the individual, the

intrinsic digestibility of the food (i.e., chemical composition), and

daily intake by the bird. He observed that digestive and absorptive

abilities of birds varied as much intraspecifically as


Karasov (in press) summarized Moss's (1983) model of digestion

based on morphology and physiology of the digestive tract and made

explicit the contribution of retention time (T) to digestibility

D a (T *k *A)/I. (4)

A general correlation of surface area of the gut and body size was

identified in passerines and nonpasserines (Karasov in press).

However, he found that retention time varies with diet type (e.g.,

grains, insects, herbs, etc.) and, to some extent, body size.

Absorption rate, a poorly known characteristic of digestion, appears to

vary with species and substrate. Thus, he concluded that each variable

must be measured before inclusion in the equation, rather than

predicted from relationships with other variables, because of complex

relationships of body size, diet specialization, and digestive


Food chemistry. Several equations have been presented to relate

metabolizable energy in poultry feeds to the physical and chemical

composition of diets, including bulk density, gross energy, crude

protein, ether extract, crude fiber, ash, starch, soluble sugars, and

tannins (Sibbald 1975). A basic assumption of these equations is that

all proteins, carbohydrates, and fats are equally digestible. The

estimates are rapid and therefore useful to the poultry industry.

However, few equations are actually used because the baseline data

obtained by agricultural researchers often are not applicable to

typical poultry farming conditions (Sibbald 1980).

The Van Soest method of forage chemical analysis (Goering and Van

Soest 1970) provides a reliable method for predicting forage digestion

and absorption in both ruminant and monogastric mammals (Van Soest

1967, Mould and Robbins 1982) and may be useful for birds as well

(Servello et al. 1987). Structural carbohydrates (fibers) in a diet

affect both digestibility and amount of feed consumed by the animal

(Church 1988). The Van Soest method determines neutral detergent fiber

(NDF: cellulose, hemicellulose, lignin, cutin, insoluble ash), acid

detergent fiber (ADF: cellulose, lignin, cutin, silica), and acid

detergent lignin content of the feeds. Lignin and ADF contents of

feeds are considered to be indicators of relative digestibility and

absorption, whereas NDF content is more often considered an index for

predicting intake (Church 1988). The method is empirical because feed

composition and the digestive/absorptive efficiencies of the animal for

classes of structural carbohydrates must be determined prior to

predicting the digestibility of alternative diets.

An equation was presented by Karasov (in press) to express

metabolizable energy coefficients (MEC) in birds as a function of the

composition of the diet, building on previous models for poultry and

fish (Sibbald 1975, Jobling 1983). Four aspects of diet (gross energy,

proportion of the diet that is not digestible and its energy content,

and proportion of the diet that is nitrogen), and 3 aspects of the bird

(energy loss in endogenous materials, energy loss due to excess

nitrogen in the diet, and intake), were combined to predict the MEC of

birds on specific diets. Agreement of predicted and empirical MECs was

good for 4 of 7 diet types (i.e., good agreement for nectar, vertebrate

prey, domesticated and wild seeds, but not good agreement for arthropod

prey, fruit, or grasses) in interspecific comparisons. However,

difficulties existed in predicting proportions of diets that are not

digestible. The recurrent problem of predicting digestible fractions

of diets again supports the idea that more data are needed by means of

diet testing prior to understanding how different species digest

different foodstuffs.


Most models for digestion have dealt not only with digestion, but

with the combined events of digestion and absorption as means to

improve net energy or nutrient gain by an animal. The concept of a

digestive strategy provided a framework for understanding the

relationships of gut size, retention time, and food selection.

Optimality modelling predicted that 2 parameters of digestion should be

most significant to the digestive processes of an animal as a means to

alter net energy gain: gut volume and retention time. Empirical models

based on anatomy and diet corroborated the importance of gut volume and

retention time to altering net energy gain from digestion, but added

the parameters of intake, rates of absorption, and chemical composition

of the foods to the general predictive models. The latter 2 parameters

must be measured in each species for each nutrient and diet prior to

inclusion in models of digestibilities/absorption. Flexibility in each

of these features may enable an animal such as an omnivorous bird to

maintain net gain of energy and nutrients when the environment or its

metabolism change.

Red-Winged Blackbirds: Diet Generalists

Red-winged Blackbirds are omnivorous passerines. Given a broad

diet, redwings should exhibit characteristics of digestive flexibility:

variable intake, gut volume, and retention with a shift in diet from

one food type to another. A brief summary of existing information

about the food habits, gut morphology, and energetic of Red-winged

Blackbirds will provide a perspective from which to view the feeding

experiments of this study.

Food Habits

There is an extensive literature summarizing the food habits of

Red-winged Blackbirds (see Crase and DeHaven 1975 for a review). Most

studies quantify diet during summer months or during seasons of bird

damage to crops, such as planting or harvest, because migratory

populations are present only during those periods. Redwings are

primarily granivorous in autumn, winter, and spring, and switch to a

diet dominated by insects during summer (Beal 1900). Marsh nesting

birds may consume invertebrates exclusively during breeding season,

whereas upland nesting birds may consume variable proportions of grain

and animal matter (Bird and Smith 1964). Redwings also consume fruits

(Allen 1914), vegetables (tomatoes, pers. obs), and nectar (pers.


Anatomy of the Gastrointestinal Tract

The digestive tract of the Red-winged Blackbird has a relatively

simple anatomy: the buccal cavity and pharynx; the esophagus and crop;

the stomach, which is composed of the proventriculus and gizzard; the

small intestine; the paired ceca; the large intestine; and the cloaca.

Associated with the digestive system are glands such as the liver and

pancreas, which secrete products to the duodenum.

The esophagus is thin-walled with a diverticulum, or spindle-

shaped crop (McLelland 1979), that lies to the right of the trachea.

The crop is formed by folds that allow expansion of the middle

esophagus. When full, the crop wraps around the right side of the neck

and forms a bulge at the right and back of the neck, similar to that

described for Redpolls (Fisher and Dater 1961). In adult males, the

esophagus extends approximately 60 to 75 mm from mouth to

proventriculus. Cervical and thoracic diameters of the esophagus are

approximately 3 mm. The inner diameter of the flattened crop is

approximately 15 to 20 mm. The maximum volume of food I have found in

the esophagus of a redwing was approximately 2 ml. This specimen was a

second-year male in late winter and collected just before nightfall

(Brugger, unpubl. data).

The proventriculus, or glandular stomach, is a thick-walled

enlargement of the digestive tract approximately 7 mm long. Inner

diameters of the proventriculus range from 1.5 to 2 mm. Food is rarely

found in this portion of the gut during post-mortem examinations. The

gizzard, or muscular stomach, is a saggitally flattened sphere,

approximately 15 to 20 mm in diameter. It lies to the lower left of

the heart, and is covered ventrally by lobes of the liver. A tendinous

layer covers the center of each side of the gizzard. Muscle layers are

thickest at the rim of the gizzard. The gizzard may hold up to 0.5 ml

of digest (Brugger, unpubl. data).

The small intestine of adult males is approximately 2 to 5 mm in

diameter and 160 to 240 mm long. Thickness of the intestine wall

varies along its length. It is thinnest in the proximal duodenum, and

again at the ileum. Pancreatic and bile ducts enter the intestine

along the distal loop of the duodenum. Up to 0.5 ml digesta may be

carried in the small intestine (Brugger, unpubl. data).

The ceca are paired, 2 to 8 mm diverticula at the juncture of the

small and large intestines. Often the left cecum is longer than the

right by 1 to 2 mm. Only watery and mucous materials have been found

in the ceca.


The large intestine and cloaca are thin-walled structures

approximately 5 to 8 mm in diameter, with a combined length of 15 to 20

mm. Digesta typically are expelled from the large intestine and cloaca

at death; hence, these regions are often empty at post-mortem


A correlation between food habits and gut size was found in a

collection of wild redwings made during late winter and spring in

Louisiana (Brugger and Martinez del Rio 1988). Seeds were the most

abundant food in gut contents of birds collected in late winter;

insects comprised the largest proportion of gut contents in spring.

Winter-collected birds had longer small intestines than did birds

collected in spring. These results suggested that a dynamic change in

gut volume occurred with seasonal shift in diet.


Redwings are sexually dimorphic in body size, with females smaller

than males. Body mass varies with latitude. Mean mass of adult males

is 55 g in Florida (Brugger, unpubl. data) and 81 g in Saskatchewan

(Power 1970); females weigh 36 g and 54 g in these locations,

respectively. Mean body temperature varies directly with ambient

temperature, ranging from 38.5 OC to 41.5 OC as ambient increases from

5 oC to 40 OC (Lustick 1975).

Rates of metabolism, as measured by standard metabolic rate (SMR)

(i.e., fasting, inactive birds at known body temperature) show a

curvilinear response to temperature during the day, and a linear

response at night (Lewies and Dyer 1969). A thermal neutral zone


exists at ambient temperatures ranging from 200-40 oC, depending on

time of year that birds are tested, molt, body condition, and

physiological parameters that might affect conductance (Brenner and

Malin 1965, Lewies and Dyer 1969, Lustick 1975). Observed SMR at 24 OC

was 1.108-4.692 cc 02/(g*h) for adult male redwings (Brenner and Malin

1965). Expressed in energy, mean daytime SMR of adult males is 60.36

J/(g*h), and mean nighttime SMR is 39.33 J/(g*h) at 24 oC (Lewies and

Dyer 1969). Thus, daily expenditure at SMR for a 60 g adult male

redwing exposed to a photoperiod of 12L:12D is expected to be

approximately 66 kJ. In mammals and birds, average daily metabolic

rates, also termed daily energy expenditure, may range from 1.5 to 4

times SMR (King 1974, Drent and Daan 1980), with a maximum daily energy

expenditure that may reach 5 times SMR (Kirkwood 1983). Thus, an adult

male redwing at 24 oC could require a daily rate of energy intake

ranging from 99 to 264 kJ, with a maximum of 330 kJ. This amount would

be higher at temperatures below 24 oC.


Four separate feeding experiments were conducted. In the first

experiment, I tested for effects of diet quality on digestibilities and

gut anatomy. Three diets that varied in relative energy content by

mass were tested. In the second experiment, I tested for circannual

fluctuation in digestive and morphological responses by offering birds

a single controlled diet and exposing them to natural seasonal

variation in daylength and temperature. Four seasonal treatments were

conducted in sequence. In the third and fourth experiments, I tested

the effects of daylength and air temperature, respectively, on

digestive and morphological responses. Two photoperiod and 2

temperature treatments were used.

Birds used in the feeding experiments were captured from the wild

and allowed to acclimate to captivity prior to testing. A test

consisted of placing birds in separate cages, and feeding them test

diets for at least 2 wks. Complete collections of food and feces were

made during 3-day digestion trials, allowing direct measurements of

digestive responses. An estimate of retention time was obtained once

per day for 2 or 3 consecutive days prior to a digestion trial by

measuring transit time. Birds were killed after a digestion trial for

measurement of internal organs.

General Procedures


Male Red-winged Blackbirds used in the feeding trials were

captured within 10 km of Gainesville, Florida, during March 1986 and

November 1987 in decoy traps operated by the United States Department

of Agriculture/Denver Wildlife Research Center (USDA/DWRC) (U. S.

Department of Interior, Fish and Wildlife Permit No. PRT-680104).

Birds were transported to the outdoor aviary of the DWRC Florida Field

Station, weighed, and measured for 3 characters: wing chord; bill

length; and tarsus length (Baldwin et al. 1931). Birds were then

marked with individually numbered aluminum leg bands. Only after-

second year males of a standard body size that suggested they were from

small geographic area were used in feeding trials to reduce potential

variance in digestive processes associated with age (Kendeigh et al.

1977) or genotype (Blem 1973). Birds were selected for study if body

mass was between 52 g and 60 g, and wing chord (distance from the

anterior edge of the "wrist" joint to the tip of longest primary) was

less than 118 mm, following the measurements of Howe et al. (1977) for

Florida birds.


During a 1-mo period of acclimation to captivity, redwings were

housed in 1.2 m3 cages of wire mesh, outfitted with 2 or 3 metal

perches that extended the length of the cage. Birds were given water

and Purina Layena chick layer mash ad libitum. Redwings suffered an

initial mortality of approximately 10% during the first month of

captivity (USDA/DWRC unpubl. data). Thereafter, remaining birds

survive 2 to 4 years in captivity.

Prior to feeding experiments, an estimate was obtained of the time

required for individual birds to acclimate to the study cages (45 cm x

45 cm x 90 cm) and test diets. A bird was considered to be acclimated

to the new cage and diet when intake and body mass stabilized. Ten

adult male redwings were taken from the 1.2 m3 group-holding cages, and

placed in individual wire-mesh study cages during May 1987. They were

provided the maintenance diet and water ad libitum. Daily measures of

individual food intake and body mass (to the nearest 0.5 g) were taken.

Body mass was measured at dawn, prior to the first meal or drink of the

day, presumably when the gastrointestinal tract was empty. An

acclimation period of two weeks was sufficient to obtain stable daily

intake and body mass, and was used thereafter for all feeding trials.

Digestion Trials

A bird was removed from the group holding cage, weighed, checked

for overt signs of illness, and, if apparently healthy, placed in an

individual holding cage. During the 2-wk acclimation period, birds

were fed their test diet and water ad libitum. Body mass was measured

at dawn every other day. At the end of 2 weeks, if body mass was

stable (indicating a balanced energy budget, Kendeigh et al. 1977), a

3-day digestion trial was begun.

On the first day of a digestion trial, the bird was weighed, and

an aluminum pan with plastic liners was placed in the cage bottom

through a port at the back of the cage. Thereafter, food was offered

in portions of known mass. Food was dried at 40 oC to constant weight

(approximately 48 h). Dry food samples were weighed at least 24 h

prior to a trial, and allowed to rehydrate to ambient humidity before

being offered to a bird. Leftover food and plastic cage liners were

removed daily at dawn. The products of the excretory system (uric

acid) could not be separated from that of the digestive system (feces);

hence, they were treated together. Hereafter, the term "feces", as

applied to these collections, will be used to denote the combination of

feces and uric acid. Spilled food and feces were separated and scraped

from the plastic liners. A small film of uric acid residue remained on

the plastic sheets after scraping. No correction was made for this

remaining uric acid. Instead it was assumed that the errors in energy

and nitrogen estimates introduced by the inability to remove all uric

acid were similar among birds.

All samples were dried at 60 oC for 48 h before weighing. Daily

dry-matter intake was calculated as the difference between dry masses

of food offered and that leftover and spilled. Samples of leftover

food, spilled food, and feces were stored frozen in inert plastic bags

for later analyses.

Study Design

Experiment I: Diet Ouality

Diets. The concept of diet quality must be clarified.

Qualitative differences in diets encompass physical and chemical

composition, voluntary levels of intake, and digestibilities of energy

or nutrients in relation to the physiological status of the animal (Van

Soest 1982). Two definitions of diet quality were presented in models

of digestion: Milton (1981) defined diet quality by energy density;

Sibly (1981) stated that diet quality was determined by the net gain of

energy or nutrients over time. By the latter definition, a poor- or

low-quality diet could be energy- or nutrient-dilute, take a long time

to digest and absorb (Martinez del Rio and Karasov, in press), provide

unavailable or imbalanced nutrients (Robbins 1983), be unpalatable, or

be ecologically unavailable (Van Soest 1982).

Commercial diets were used in this experiment, so I assumed that

diet quality was not affected by problems of digestibility, nutritional

balanced, palatability, and limited quantities as listed above. For

the purpose of the feeding experiment, I will use only energy density

as the criterion to determine diet quality. Therefore, the diet that

is most dilute (by mass) in energy will be termed the lowest quality


Diets were selected for testing that represented variation in

energy and nutrient contents likely to occur in the natural diets of

Red-winged Blackbirds. The seasonal range in chemical composition of

natural diets was estimated by nutritional analyses of samples of gut

contents taken from 10 adult male Red-winged Blackbirds collected 20-24

March and 10-15 April 1987 in southwestern Louisiana (Table 1).

Redwings diversify their diets during this time, expanding from

primarily domestic grains to a combination of wild seeds, other

vegetable matter, invertebrates, nectar, and fruits (Kalmbach 1937).

Also, the nutrient compositions of representative seeds (barnyard

grass, Echinchoa cruS-galli) and invertebrates that might be consumed

by redwings were obtained from the literature for comparison with data

of gut contents (Table 1) to establish a range of diet qualities that

redwings could encounter.

Commercial diets were selected for use in the feeding experiment.

Purina Layena contained the lowest energy concentration and Flint

River Mills (FRM) Game Bird Grower the highest of available commercial

diets. These were selected for use as the low-quality (L) and high-

quality (H) diets. The medium-quality diet (M) was formed by diluting

the FRM Game Bird Grower diet to obtain a diet with intermediate

energy contents by mass. Mahogany (Swietenia spp.) sawdust was used as

a diluent because of its high lignin content (26%), which was presumed

to be indigestible by redwings (Savory and Gentle 1976b). I used a

ratio of 1:6 sawdust:feed.

The diets represent qualitative differences beyond that of simple

concentrations of energy. Variable amounts of corn, soybeans, and

supplements were used by the commercial feed producers as carbohydrate

and nitrogen sources (K. Houseman, Purina, and H. Metcalf, FRM, pers.

Table 1. Nutrient composition of (1) contents of the esophagus and
gizzard of 10 adult male Red-winged Blackbirds collected 20-24 March
and 10-15 April, 1987, in Louisiana, (2) natural foods (seeds,
invertebrates [inverts.]), (3) maintenance diet, and (4) experimental
diets fed to adult males. Nutritional analyses are organic matter (OM)
as percent of wet weight, energy content of dry matter (DM), and
nitrogen (N), ash-free neutral detergent fiber (NDF), acid detergent
fiber (ADF), and lignin (Lig), reported as %DM. Volume of DM is
reported for the maintenance and experimental diets. Number of
treatments per feeding experiment is given in parentheses. A dash (-)
indicates data not obtained.


OM Energy N NDF ADF Lig Volume
Foods (%) (kJ/g) (%) (%) (%) (%) (ml/g)

(1) Gut Contents
March 89.7 17.5 2.1 28.2 -

April 88.2 18.8 4.0 25.7 -

(2) Natural Foods
Seedsl 89-97 16.1 1-3 8-30 -

Inverts2 92-98 21-24 9-12 3-503 -

(3) Maintenance Diet
PL 85.7 16.3 2.8 20.0 9.8 2.8 0.5

(4) Experimental Diets
I-Low-PL (1) 83.6 16.2 3.0 23.1 9.8 2.9 0.5

I-Medium (1) 90.2 18.4 3.8 31.0 17.5 4.9 0.7

I-Sawdust 82.0 16.6 0.4 89.5 80.3 26.1 1.9

I-High (1) 91.5 18.7 5.5 18.8 9.0 2.1 0.5

II-PL (4) 85.0 16.6 2.8 20.0 7.5 1.4 0.5

III-PL (2) 87.3 16.8 2.9 17.7 9.7 2.8 0.5

IV-PL (2) 82.1 16.7 2.7 20.0 6.8 1.5 0.5

1 Data for hulled seeds of barnyard grass, Echinochloa crus-gallii (Duke
and Atchley 1986).
2 Data for isopods, homopterans, coleopterans, formicids, dipterans,
and arachnids from Stiven 1961, and energy content from Bernays 1986.
3 Crude fiber.

comm.). Flint River Mills often uses molasses as a carbohydrate, which

must be hydrolyzed prior to absorption, possibly slowing net energy

uptake. The diets differed in nitrogen content and likely differed in

biological values of protein, possibly affecting uptake of nitrogen.

The fiber content and volume of the medium-quality diet were the

highest values of the 3 diets (Table 1), possibly depressing overall

digestibility of the medium-quality diet. Thus, many facets of these

diets could influence digestive performance.

Procedures. On 30 June 1987, 66 birds were placed in separate

cages and, for a 2-wk acclimation period, fed from the same batch of

Purina Layena. Twenty-two birds were assigned randomly to each of 3

treatments (low-, medium-, or high-quality) prior to the feeding

trials. After the 2-wk acclimation period, birds assigned to the

medium- and high-quality diet treatment groups were given the new

diets, while birds in the low-quality diet treatment continued on the

Purina Layena, thus serving as a control group. Four birds per diet

were assigned to each of 4 sampling periods for digestion trials (p.

23), which were conducted days 1-3, 6-8, 15-17, and 34-36 after

introduction to the new diets. Each bird was sacrificed between 1200

and 1600 the day after its 3-day digestion trial for measurement of the

gastrointestinal organs. The remaining 6 birds per diet treatment

formed a fifth sampling group. They were not included in digestion

trials, but intake of each was measured on days 37-39. These birds

were sacrificed for measurement of gut anatomy on day 40.

Experiment II: Season

Four times over the course of a year (20 May 1988, 25 August 1988,

16 November 1988, and 5 February 1989), groups of 12 birds were taken

from outdoor holding pens, where they had been exposed to natural

seasonal variation in daylength and temperature and fed the common

maintenance diet. They were placed in individual digestion cages in

the same outdoor aviary and exposed to natural daylight and

temperature. Birds were thereafter fed from a single batch of Purina

Layena (labeled "II-PL" in Table 1). This diet was kept frozen

between feeding trials to prevent degradation. Three-day digestion

trials began 2 weeks after birds were placed in the cages.

Experiment III: Photoperiod

On 5 January 1988, 24 birds were taken from outdoor holding cages

and placed in separate wire cages in environmental chambers at 20 C

under 1 of 2 photoperiod treatments, 9 L:15 D or 15 L:9 D. These light

cycles were chosen to match the extremes to which Florida redwings

would be exposed in mid-winter and mid-breeding season, respectively.

Birds were fed ad libitum food from another batch of Purina Layena

(labeled "III-PL" in Table 1) and held under their respective light

regimes for 30 d.

The long-day cycle was planned to be sufficient to elicit

measureable testis growth (Payne 1969:90). Blood samples were taken

from each bird for analysis of testosterone (Wingfield and Farner 1976,

Diagnostic Products Corporation 1988) to see if developing testes were

hormonally active. Baseline estimates of the sizes of testes and

gastrointestinal organ were obtained by sacrificing 6 birds per

treatment at the end of 30 days. The remaining 12 birds were included

in 3-day digestion trials, after which they were sacrificed and the

sizes of testes and gastrointestinal organs measured.

Experiment IV: Temperature

On 1 November 1988, 24 birds were taken from the outdoor cages and

placed in separate cages in 1 of 2 environmental chambers set at a

common light cycle of 12 L:12 D and at 1 of 2.air temperature

treatments, 20 OC or 7 OC. The former air temperature fell within, and

the latter temperature below, the thermoneutral zone (Lustick 1975,

Brenner and Malin 1965), thus representing differing energy demands.

Birds were fed Purina Layena ("IV-PL", Table 1) and held in the

chambers for 30 days. Six birds per treatment were sacrificed at the

end of 30 days and gut sizes measured. The remaining 12 birds were

included in 3-day digestion trials, and sacrificed thereafter.

Measurements and Analyses

Retention Time

Retention time of digesta was measured in subsamples of birds in 3

feeding experiments. I used transit time, defined as the time between

first consumption of marked food and first appearance in the feces, as

an estimate of retention in Experiments II, III, and IV. The measure

of transit time was chosen because diet did not vary among treatments

in these 3 experiments, and presumably, the shapes of the retention

curves did not vary (Kotb and Luckey 1972, Warner 1981). Thus, the

time of first appearance of markers in the feces would estimate

relative differences in speed of food passage, when diets are

identical. No estimates of retention time were made for Experiment I

because of difficulty in satisfactorily marking diets that differed in

physical and chemical composition.

Transit time was estimated once per day for 2 to 3 consecutive

days prior to a 3-day digestion trial, using a dyed-food method. Two

dyes were tested; commercial blue food coloring was used in Experiment

II and Phenol Red was used in Experiments III and IV. Fifty g of dry

maintenance diet was soaked for 15 min in a 10 ml solution of (a) water

and 5 drops of blue commercial food coloring, or (b) 5% Phenol Red by

volume. The mixture was then dried to constant weight at 40 oC for 48

h. At 1000 on the test morning, the trays of partially eaten, undyed

maintenance diet, which had been placed in the cages at approximately

0800, were removed from the cages of 6 birds. At 1200, they were

replaced with a tray of dyed food. Cages were scanned continuously for

2.5 h to identify the time of first food consumption and time that dyed

feces appeared on the metal shelf below the cage. Transit time was

calculated as the time that elapsed between first observation of

feeding from the dyed food and first traces of color in the feces.

The test birds were food-deprived for 2 h to ensure that they

would readily take the dyed food and to improve the likelihood that

time of first food consumption would be observed. Food deprivation

could result in biased transit times by speeding flow-through of

digesta because peristalsis and intestinal secretions increase in

fasted birds (Duke 1984). However, redwings naturally feed in pulses

during the day with 1-4 h intervals between bouts of foraging (Hintz

and Dyer 1970). Thus, a 2-h food deprivation period fell within the

range of natural foraging patterns by these birds, possibly yielding

data for captive birds that were comparable to wild birds.

Gut Anatomy

At the end of a digestion trial, each bird was killed by C02

overdose (University of Florida Animal Care Committee permit), weighed

( 0.01 g), and dissected of the gastrointestinal tract. Measurements

were taken of empty, rinsed organs as follows: outside width and length

of gizzard, depth of thickest wall of gizzard, and mass of gizzard

(patted dry with a paper towel); small intestine length (SIL), width of

split intestine (-inner circumference), and mass of small intestine

(patted dry); lengths of ceca; and large intestine length (LIL). Two

methods to determine length of small intestine were compared: slipping

the intestine over a 2 mm diameter metal rod and allowing it to recoil

to a relaxed shape; and attaching a Pesola scale to one end and

allowing the intestine to stretch freely with a 5 g tension (Freehling

and Moore 1987). The former method was more precise on fresh tissue

than the latter and was used consistently in subsequent experiments.

The 3 linear measures of gizzard size (width, length, and wall depth)

were intercorrelated with gizzard mass. Hence, in the results section,

only gizzard mass will be presented. Repeated measures of the width of

specific locations and mass of the small intestine had very high

errors, probably due to drying and shrinkage of the tissue. These

measures also will not be presented in the results section because they

may be inaccurate.

Histological preparations were made of transverse sections of

tissue taken from the first 2 cm of the duodenum in 4 birds per diet

from the fifth sampling period of the diet quality feeding trial to

determine if adaptation to diet occurred in intestinal villi. Tissue

was preserved in neutral buffered formalin, imbedded in paraffin, and

sliced to 8 Jm sections. Harris hematoxylin, Biebrich scarlet/orange

II, and fast green stains were used (Humason 1972). The depth of the

basement membrane, the depth of the crypts of Lieberkuhn, the length of

intestinal villi, and the diameter of the lumen were measured with an

ocular ruler in 5 histological sections per bird at a magnification of

40X (Hodges 1974).

Food Assimilation

Nutritional analyses. Samples were ground in a Wiley mill to pass

through a size 20 screen. Diet volume was measured by water

displacement (Tarpey 1965). Energy content of samples was determined

by adiabatic bomb calorimetry, with acid and fuse corrections (Parr

1960). Approximately 1 g of sample was burned under 25 psi oxygen.

Dry matter (DM) was determined by drying 1 g of material in an oven at

105 OC for 8 h (AOAC 1960). Water content was measured by the

difference in mass of the sample before and after drying. The ash

(inorganic matter) content was determined by ignition of the DM sample

at 500 oC for 3 h (AOAC 1960). Fiber was determined by the neutral

detergent method (Goering and Van Soest 1970), with amylase

predigestion (Van Soest and Wine 1967, Robertson and Van Soest 1977),

and is reported ash-free.

The nitrogen (N) fraction was determined by a semi-automated

Kjeldahl procedure (Wall and Gehrke 1975, Technicon Industrial Systems

1977). An estimate of crude protein in the diet was not calculated

because amino acid contents of the diets were not known and because

there is a range of conversion factors among food constituents (Milton

and Dintzis 1981, McDonald et al. 1988). In addition, monogastric

animals, including domestic fowl, are not capable of using most

nonprotein nitrogen compounds such as free amino acids, amides,

ammonium salts, secondary compounds, and urea (Bondi 1987). Hence, an

estimate of crude protein based on the typical conversion of 16%

nitrogen in protein would offer misleading information about protein

digestibilities and was not used for the study.

Digestibilities. In this study, the term digestibility will be

used to denote the proportion of energy or nutrient that is apparently

assimilated relative to that consumed. It is calculated by the

equation presented for apparent assimilation efficiency in energy


Apparent = (I (F + U)) 100%
Efficiency I (5)

where I is energy in intake, F is energy in feces, and U is energy in

excreta, or urinary products (Merker and Nagy 1984). Because urine was

included the collections of feces of redwings, these collections

account for the value (F + U).

Two measures of digestibility were used, metabolizable energy

coefficient (MEC), and assimilable mass coefficient (AMC). Each are

termed "apparent" because it is not possible to separate feces from

uric acid in the droppings. Hence, materials of endogenous origin,

such as the lining of the gut, and urinary products (both of which were

previously digested, absorbed, and metabolized) were included in the

determinations. Thus, apparent MECs and AMCs probably underestimate

actual digestibilities. The metabolizable energy coefficient (MEC)

refers to the proportion of digestible energy that can be metabolized.

The apparent metabolizable energy coefficient is calculated with

equation (5), substituting energy content (kJ/g) for nutrient mass.

The AMC of a nutrient is the proportion of ingested nutrient, measured

on a dry matter basis, that is apparently assimilated by the animal.

The assimilable mass coefficients for OM, N, and NDF were calculated

with equation (5) using dry mass of nutrients in the diet and feces.

The ingested or defecated dry mass of the nutrient was determined by

multiplying its proportion in the diet or feces by the amounts of diet

ingested or feces expelled.

The digestibility of nitrogen (AMC-N) is considered an

inappropriate measure to use in digestion studies of birds because

nitrogen flux is dependent on the energy balance of the animal, the

biological values of the proteins in which nitrogen is bound, and

methods for nitrogen conservation in the animal. Energy demand and

tissue turnover can be particularly high in birds because of small body

size and relatively high metabolic rates (Robbins 1983). Protein is

catabolized for energy if the animal is unable to meet energy demands

by diet, alone. Thus, excess nitrogen may be excreted when proteins

are catabolized for energy, resulting in an underestimate of the

measure of AMC-N.

An alternative measure of nitrogen flux is termed nitrogen

balance. It estimates the amount of nitrogen retained in the bird.

Nitrogen balance is calculated by the equation (In (Fn + Un)), where

In-nitrogen intake and (Fn + Un)=nitrogen in feces and urine. Both

measures of nitrogen flux will be presented for heuristic value and

will be discussed in reference to eachother.

Data Analyses

Energy and nitrogen balance. Only data from birds that were in

energy balance and positive nitrogen balance are reported for the

feeding trials. These criteria resulted in 5 birds being dropped from

study, all in Experiment II. A bird was considered to be in energy

balance if body mass variation was within 2.5% during the acclimation

period prior to a 3-day digestion trial (Kendeigh et al. 1977). A bird

was considered to be in positive nitrogen balance if the calculated

value was >0 (Harris 1966).

Nutritional analyses. In all analyses, except that of nitrogen,

independent replicates were acceptable with a relative error of 2%,

Error = ([Replicate 1 Replicate 2]/Replicate 1) 100%. (6)

If the replicates were not within 2%, then a third replicate was

analyzed (AOAC 1960).

The relative errors for nitrogen estimates were high.

Nonindependent estimates taken from triplicate readings of single

samples averaged a relative error of 6% (n=40) and decreased

logarithmically with increasing nitrogen content. The within-sample

error was attributed to the automated procedure of light absorbance

readings. Thus, independent replicates of nitrogen analyses were

acceptable at the mean level of within-sample relative error, 6%.

Statistics. A standard software package, Systat (Wilkinson

1987), was used for statistical analyses, which primarily included

summary statistics, t-tests, linear and nonlinear regressions, and

analyses of variance (ANOVA) and covariance (ANCOVA). Homogeneity of

variance among treatment groups was evaluated with Bartlett's test (Zar

1984). An arcsine squareroot transformation was applied to

digestibility data to meet the assumptions of homogeneity of variances

and normality. Unless otherwise noted, I present data from independent

samples taken from separate individuals in each feeding trial.

An ANCOVA was used, with body mass as the covariate, to test for

allometric effects on dependent variables in all experiments.

Dependent variables tested were daily dry matter intake, daily dry

matter defecation, energy concentration in feces, MECs, assimilable

mass coefficients of OM, N, and NDF, anatomical measures, and daily

metabolizable energy intake (MEI)

MEI = I (F + U), (7)

where I=energy consumed and (F + U)=energy defecated and excreted.

A 2-way ANOVA was used in Experiment I to test for the main

effects of diet (3 diets) and time (4 sampling periods) and their

interaction on dependent variables. A nested 1-way ANOVA was used to

test for differences among fixed diet treatment groups in intestinal

histology, using the 5 sections per bird as random repeated measures

within the random variable of an individual bird. The nested repeated-

measures ANOVA was used to allow for variability in the measurement of

villus length within replicates (a single bird).

A 1-way ANOVA was used in Experiment II to test among the 4

seasons for differences in the above listed dependent variables. An

analysis of covariance (ANCOVA) was used to test for differences in

mean MECs and AMCs among seasons, controlling for intake. An ANCOVA

preliminary model was used to test an assumption of ANCOVA that there

is no significant effect of the interaction of season and intake (the

covariate) on MEC or AMC (Sokal and Rohlf 1981). A significant effect

would indicate that the MEC/intake slopes (or AMC/intake slopes) were

not equivalent among seasons. Nonequivalence of slopes would render

the ANCOVA invalid as a test for differences in mean MECs or AMCs among

seasons when intake is controlled.

Multiple comparisons of data from the diet and season experiments

were performed with t-tests, using Bonferonni's adjustment (a/k) to

account for experimentwise error, where k is the number of comparisons

being made. The t-tests conserve power by reducing the number of

comparisons to a meaningful subset, and reduce the overall comparison

error rate for multiple hypotheses (Carmer and Swanson 1973).

One-tailed t-tests were performed for 3 diet comparisons (L, M;

L, H; and M, H) irrespective of sampling period (Petersen 1977).

Directional predictions for responses were as follows. Nitrogen

balance should be directly related to a ratio of nitrogen:energy,

following the pattern of H>M>L. Body mass should remain identical

among diets, L-M-H. Intake should be inversely related to energy

density of the diets, following the pattern of L>M>H, and MEI should be

a product of intake compensation and energy densities of the diets,

following a pattern of H=M-L. Dry mass defecated should be directly

related to intake, following the pattern L>M>H. Digestibilities of

energy, OM, and N should be directly related to their concentrations in

the diet, following the pattern of H>M>L. Fiber digestibility should

be negligible for all diets, following a pattern of H-L-M. Anatomical

measures should be directly related to intake, following the pattern of


Two-tailed t-tests were performed for digestive and anatomical

responses irrespective of diet between the first and second, and first

and fourth sampling periods, only. The temporal comparisons were

chosen to identify the potential for short-term (days) and long-term

(weeks) acclimation to the treatments.

Additional one-tailed t-tests were performed for histological

responses between high- and low-quality diets and high- and medium-

quality diets, but not the low- and medium-quality diets. I reasoned

that the high- and low-quality diets differed by many facets of food

chemistry, because they were feeds formulated by different companies.

Thus, the high-low pairwise comparisons might reveal differences in

redwing responses to the commercial feeds. The high- and medium-

quality diets were variants on the same diet, differing only by a 14%

dilution with sawdust. Thus the high-medium pairwise comparisons might

reveal specific effects of fiber dilution on digestive histology.

Directional predictions were based on the predicted pattern of intake,

which was L>H and M>H. Histological measures should be directly

related to intake, following the pattern L>H and M>H.

In Experiment II, one-tailed t-tests were used to contrast summer

responses (August) with those of winter (February) and summer with

spring (May). Metabolic demand for heat production should be lowest in

summer and highest in mid-winter. Daylength for feeding and other

activities is shortest in winter. Thus, a pairwise comparison between

February and August would reveal directional differences in digestive

responses associated with the effect of extreme combinations of

temperature and daylength on intake. Intake should be higher in

February than August, thus digestibilities should be lower and measures

of gut organ sizes should be greater in February. Temperature and

daylength are similar in May and August, but birds are in breeding

condition and possibly more active in May. Therefore, intake should be

higher in May than August, digestibilities should be lower, and

measures of gut organ sizes should be greater in May.

One-tailed t-tests were used in the photoperiod and temperature

experiments to test for differences between treatment means. I

predicted that intake would be greater for birds on the long-day cycle

and in the low temperature chamber, with digestibilities inversely

related to intake and anatomical measures directly related to intake.

For all experiments, the a level was set a priori at P0.05.

Comparative differences of means that are reported in units other

than % were calculated with respect to the lowest value, following

equation 6. Comparative differences of digestibilities, reported as %,

are reported as the absolute difference between the means.


Experiment I: Diet Ouality

Complete measures were made with 48 birds. All birds were in

energy balance prior to the experiments and positive nitrogen balance

during the experiments (Table 2). There were no allometric effects on

the digestive and anatomical response variables in the first four

sampling periods.

Nitrogen Balance and Body Mass

Nitrogen balance differed significantly among diets (P<0.01), but

not sampling periods (P=0.35, Table 2). No interaction of diet and

sampling period was observed for nitrogen balance (P=0.89). Birds on

the high- and medium-quality diets consumed more nitrogen per day than

those on the low-quality diet, yielding a pattern among diets of H>M>L

for nitrogen balance (all P<0.01, Tables 2 and 3). Nitrogen balance

never exceeded +0.5 g/day (Table 2, Fig. 2A).

Results of 2-way ANOVA revealed that, during the experiment, mean

body mass of birds did not differ among diets (P=0.71, Tables 2 and 3),

but differed among sampling periods (P<0.01, Tables 2 and 4, Fig. 2B).

There was a trend (trend=0.10>P>0.05) of interaction of diet and

sampling period on body mass (P=0.07, Table 2). Multiple comparisons

Table 2. Summary statistics of diet quality experiment, mean (SE).
Three diets were tested: low-quality, medium-quality, and high-quality
(see Table 1). Abbreviations are metabolizable energy intake (MEI),
metabolizable energy coefficient (MEC), assimilable mass coefficients
(AMC) for organic matter (OM), nitrogen (N), and neutral detergent
fiber (NDF), and small intestine length (SIL). Results of 2-way ANOVA
(F-statistic, P) are presented below names of dependent variables for
main effects of diet (D, df-2), main effects of sampling period (S,
df=3), and interaction of diet and sampling period (DS, df=6). Letters
above means for all 16 birds per diet represent significant differences
as determined by multiple comparisons (see Table 3).

Dependent Diet quality
variable Sampling
2-way ANOVA (F, P) period Low Medium High

Nitrogen balance (mg)
D (F-55.5, P<0.01)
S (F-1.13, P-0.35)
DS (F-0.37, P-0.89)


mass (g)


Intake (g/d)
D (F-15.7, P<0.01)
S (F-2.62, P-0.06)
DS (F-1.24, P-0.31)

Defecation (g/d)
D (F-68.1, P<0.01)
S (F-4.48, P=0.01)
DS (F-0.87, P-0.53)

Fecal energy (kJ/g)
D (F=148, P<0.01)
S (F=2.92, P=0.04)
DS (F=1.88, P=0.11)

MEI (kJ/d)
D (F-8.45,
S (F=0.95,
DS (F-1.19,







190.0 (11.0) 240.0 (12.0)
153.0 (17.0) 268.0 ( 5.0)
155.0 (15.0) 268.0 (19.0)
195.0 (9.0) 293.0 (50.0)
173.0A (8.0) 267.0B(13.0)









158.2 (7.6)
138.3 (15.3)
139.7 (6.7)
165.8 (8.3)
150.5A (5.4)











189.2 (15.7)
181.6B (5.4)

398.0 (19.0)
368.0 (17.0)
360.0 (47.0)
408.0 (55.0)









173.0 (7.6)
150.7 (7.1)
168.2 (10.6)
163.2 (16.5)

Table 2, continued.

Dependent Diet quality
variable Sampling
2-way ANOVA (F, P) period Low Medium High

MEC (%)
D (F=68.6,
S (F-6.25,
DS (F=1.13,

AMC-OM (%)
D (F-50.4,
S (F-4.62,
DS (F-1.09,

AMC-N (%)
D (F-44.7,
S (F=2.46,
DS (F-0.84,

D (F-92.4,
S (F-2.23,
DS (F=1.18,




69.1A (0.8)




Gizzard mass (mg)
D (F-8.81, P<0.01)
S (F=2.86, P=0.05)
DS (F-1.75, P<0.14)

SIL (rnm)
D (F=4.27, P=0.02)
S (F-0.62, P=0.61)
DS (F-0.71, P-0.64)

Cecum (mm)
D (F-0.96, P-0.39)
S (F=0.53, P=0.66)
DS (F-1.81, P=0.13)

67. 0A







41.9A (1.1)





80.1 (1.3)
82.0 (1.6)
77.1 (2.3)
75.8 (2.7)
78.8B (1.1)









1,167.0A (32) 1,146.0A (49)

85.7 (1.7)
86.3 (0.8)
78.2 (2.9)
83.6 (0.8)
83.5B (1.1)


67. 0C







980.0B (29)

206.3 (10.2) 228.7 (11.4) 201.8 (10.9)
207.3 (16.3) 206.8 (4.0) 200.0 (12.4)
206.8 (2.8) 227.5 (6.6) 208.3 (8.6)
216.3 (8.5) 215.0 (6.2) 193.5 (7.6)
209.2A (4.4) 219.5AB(4.1) 200.9AC(4.7)

6.7 (0.8)
4.7 (0.3)
4.5 (0.5)
5.4 (0.5)
5.2 (0.3)

4.7 (0.9)
5.3 (0.5)
4.9 (0.4)
4.9 (0.8)
4.9 (0.3)

3.5 (0.3)
3.3 (0.9)
4.8 (0.5)
5.6 (0.3)
4.8 (0.3)

Table 3. Unadjusted results of multiple t-tests between diet means,
irrespective of sampling periods, for variables that showed significant
effects of diet from Table 2 (N=16 per sample, df=30). Diets are low
quality (L), medium quality (M), or high quality (H). Abbreviations
are metabolizable energy coefficient (MEC), and assimilable mass
coefficients (AMC) for organic matter (OM), nitrogen (N), and neutral
detergent fiber (NDF). Results are significant among 3 paired
comparisons if all P 5 0.016, following Bonferonni's adjustment (C/k or
0.05/3). The value <0.01 indicates numbers between 0.00 and 0.01.

Comparisons between diets

Dependent L and M L and H M and H

variable t P t P t P

Nitrogen balance (mg) 6.10 <0.01 10.82 <0.01 5.23 <0.01

Intake (g/d) 1.54 0.13 4.90 <0.01 3.82 <0.01

Defecation (g/d) 7.45 <0.01 10.03 <0.01 3.08 <0.01

Fecal energy (kJ/g) 14.01 <0.01 13.15 <0.01 3.40 <0.01

Metabolizable Energy
Intake (kJ/g) 4.05 <0.01 1.73 0.09 2.32 0.03

MEC (%) 7.02 <0.01 10.30 <0.01 2.32 0.03

AMC-OM (%) 6.70 <0.01 9.26 <0.01 2.37 0.02

AMC-N (%) 6.20 <0.01 9.40 <0.01 3.26 <0.01

AMC-NDF (%) 13.10 <0.01 9.73 <0.01 1.31 0.20

Gizzard mass (mg) 0.37 0.72 4.36 <0.01 2.90 <0.01

Small Intestine
Length (mm) 1.69 0.10 1.30 0.21 2.98 <0.01

Cecum (mm) 0.51 0.62 0.78 0.44 0.30 0.77

Table 4. Unadjusted results of multiple t-tests of sampling period
means within diets for variables in Table 2 that showed a significant
effect of sampling period. Abbreviations are metabolizable energy
coefficient (MEC) and assimilable mass coefficient of nitrogen (AMC-N).
Results are significant among 2 paired comparisons if both P 5 0.025,
following Bonferonni's adjustment (a/k or 0.05/2). The value <0.01
indicates numbers between 0.00 and 0.01.

Comparisons between sampling periods

Dependent 1 and 2 1 and 4
variable t P t P

Body mass (g) 0.71 0.49 1.99 <0.06

Defecation (g/d) 0.27 0.79 1.03 0.31

Fecal energy (kJ/g) 0.52 0.61 0.88 0.39

MEC (%) 0.08 0.93 1.17 0.25

AMC-OM (%) 0.10 0.92 1.02 0.32

Gizzard mass (mg) 0.54 0.59 1.71 0.10

----O--- Low
---+-- High

- ---


I0 2 3 4 5I
0 1 2 3 4 5

Sampling Period


II 2 I
0 1 2 3

4 5

Sampling Period

Mean ( SE) daily (A) nitrogen balance and (B) body mass
of adult male Red-winged Blackbirds fed 1 of 3 diets. See
Table 1 for diet contents. Four birds per sampling period
were used for estimates.








Figure 2.

among sampling periods yielded no detectable differences in body mass

(Tables 2 and 4).

Intake. Defecation. and Metabolizable Energy Intake

Results of the 2-way ANOVA showed that mean daily dry matter

intake differed among diets (P<0.01), with a trend of differences among

sampling periods (P-0.06), and no interaction of diet and sampling

period on intake (Table 2, Fig. 3A). When all sampling periods were

combined within diets, birds fed the low-quality diet consumed

significantly more (27%) dry mass per day than those on the high-

quality diet (P<0.01), birds on the medium diet consumed 20% more than

those on the high diet (P<0.01), yet there were no significant

differences in intake between low- and medium-quality diets (P=0.13,

Tables 2 and 3). These results yield an observed pattern of intake

among diets of L=M>H in contrast to the predicted pattern of L>M>H (Fig

3A). The lower mean intake in all sampling periods by birds on the

high-quality diet in comparison with those on the medium- and low-

quality diets suggests rapid short-term adjustment to energy density by

mass in the diet. In contrast, the trend of increased intake over time

by birds on the medium-quality diet suggests possible long-term

adjustment to diet volume or to the diluent.

Mean daily defecation mass differed among diets (P<0.01) and

sampling periods (P=0.01), with no interaction of diet and sampling

period (Table 2, Fig. 3B). Birds on the low-quality diet defecated 40%

more dry mass per day than birds on the medium-quality diet, and 130%

---o---- Low
*- Medium
-- -- High

" I

-k -

2 3

4 5

Sampling Period

S I -~

0 1

-........ ..........

-.. -

2 3 4

Sampling Period

Mean ( SE) daily dry matter (A) intake and (B) defecation
of adult male Red-winged Blackbirds fed 1 of 3 diets. See
Table 1 for diet contents. Four birds per sampling period
were used for estimates.




Figure 3.

more dry mass per day than birds on the high quality diet (Tables 2 and

3). Birds on the medium-quality diet defecated 30% more dry mass than

those on the high-quality diet. The observed pattern of dry mass

defecation was as predicted. The full model ANOVA showed that feces

mass differed with time; inspection of Table 2 suggests that feces mass

increased with time for birds on the low- and medium-quality diets.

However, in pairwise comparisons, defecation of dry mass did not change

significantly with time, irrespective of diet (Tables 2 and 4).

Within diets (N=16), mean daily dry matter defecation was related

to intake:

L: Defecation = 0.381*(Intake) + 0.244, r2_0.64, P<0.01; (8)

M: Defecation = 0.321*(Intake) 0.843, r2=0.34, P=0.02; (9)

H: Defecation = 0.425*(Intake) 2.220, r2=0.53, P<0.01. (10)

There were no significant differences among slopes (ANCOVA, P>0.10).

Each of the 3 intercepts did not differ significantly from 0. The

linear relationships of intake and feces indicate that passage of

digesta in the lower digestive tract does not limit intake and gut fill

within the range of voluntary consumption observed in these treatments

(Van Soest 1982: 286). These observations can be related to

predictions 1 and 2 (reviewed on pages 8-11) of Sibly's (1981) optimal

digestion model.

Results of 2-way ANOVA demonstrated that mean energy content of

the feces varied significantly among diets (P<0.01) and sampling

periods (P-0.04), with no significant interaction of diets and sampling

periods (Table 2, Fig. 4A). Birds on the low-quality diet defecated

significantly less energy per gram (19%) than those on the

-----O--- Low

S Medium
---*-- High


4 5

Sampling Period




0 1

3 4 5

Sampling Period

Mean ( SE) daily (A) energy concentration in feces and
(B) metabolizable energy intake (MEI) for adult male Red-
winged Blackbirds fed 1 of 3 diets. See Table 1 for diet
contents. Four birds per sampling period were used for


0 1





Figure 4.

I r 1 --

I -

medium-quality diet (P50.01) and less energy per gram (15.5%) than

those on the high-quality diet (P<0.01, Tables 2 and 3). Birds on the

medium diet defecated more energy per gram than those on the high-

quality diet (P<0.01), yielding an observed pattern of fecal energy

among diets of M>H>L, which differed from the predicted H>M>L (Fig.

4A). Although energy content of the medium-quality diet was

intermediate to that of the low- and high-quality diets, fecal energy

of birds on the medium-quality diet was the highest of the 3 groups.

This relationship suggests that birds on the medium-quality diet were

not able to assimilate energy relative to its proportion in the diet,

which suggests an interaction of the diluent with the feed

constituents. Sawdust may have depressed digestibility of the diet by

having a low digestibility itself, decreasing transit time, or reducing

access of digestive enzymes to nutrients. Multiple comparisons showed

that fecal energy did not differ with sampling period (Table 4).

Mean daily metabolizable energy intake varied with diet (P<0.01),

but not sampling period (P-0.42, Table 2, Fig. 4B). No interactions of

diet and sampling period on MEI were detected (P-0.34, Table 2). When

all 4 sampling periods were combined (N-16), MEI of birds on the

medium-quality diet was 21% higher than those on the low-quality diet

(P<0.01, Table 3). No differences in MEI were detected between the

low- versus the high-quality diet (Tables 2 and 3). The mean MEI of

birds on the medium diet was 11% higher than that of birds on the high

diet (P<0.03). However, Bonferonni's adjustment (a/k) reduces the P

value of the contrast, yielding the relative pattern of MEI among diets

of M>L, with H=M and H=L (Table 2). Although the energy densities of

the medium- and high-quality diets were 13.4% and 15.4% above that of

the low-quality diet, birds on the medium- and high-quality diets

decreased dry matter intake by 6.6% and 21.6%, respectively, when

compared with that of birds on the low-quality diet. Disproportionate

adjustments of dry matter intake of the fibrous medium-quality diet may

have resulted in the relative increase in MEI.


Mean apparent MECs differed among diets (P<0.01) and sampling

periods (P<0.01, Table 2, Fig. 5A). No interaction of diet and

sampling period was observed (P-0.36). Apparent MEC was 9.7% higher in

birds on the medium- than low-quality diet, and 14.4% higher for birds

on the high- than on the low-quality diet (both P<0.01), with no

differences between medium- and high-quality diets (Tables 2 and 3).

Multiple comparison with a/k adjustment yielded the pattern of mean MEC

by diet of H-M>L (Fig. 5A), in contrast with the expected H>M>L. The

t-tests showed no significant temporal difference in MECs (Tables 2 and

4). These results suggest that diet quality is of greater significance

to efficiency of energy assimilation than temporal adjustment to diet.

Regression of MEC on intake yielded no significant relationships

within diets. The lack of a relationship of MEC and intake within

diets suggested that relative availability of digesta did not limit

rates of digestion and absorption by redwings. Alternatively, lack of

a relationship between MEC and intake may be due to low variance in

intake among birds during the experiment, such that a regression could

not be established.



2 3

4 5

Sampling Period

....---- Low
-- -- Medium
---.-- High

01 I I3 4
o 1 2 3 4 5

Sampling Period

Mean ( SE) (A) metabolizable energy coefficient (MEC) and
(B) assimilable mass coefficient for organic matter (AMC-
OM) of adult male Red-winged Blackbirds fed 1 of 3 diets.
See Table 1 for diet contents. Four birds per sampling
period were used for estimates.

Figure 5.




P --.- ...

Fecal dry mass was related to MEC within diets (N-16):

L: Defecation = 15.01 13.95 (MEC), r2 0.86, P-0.04; (11)

M: Defecation = 16.06 16.36 (MEC), r2 0.85, P-0.01; (12)

H: Defecation 17.56 18.34 (MEC), r2 0.86, P-0.01. (13)

The slopes of the M and H regressions did not differ from each other

(P>0.8). The relationship of MEC with fecal dry mass suggests that

digestion and absorption rates are functionally related to the amount

of material that is defecated by the bird.

Mean AMCs of organic matter varied significantly among diets

(P<0.01) and sampling periods (P=0.01), with no interaction of diet and

sampling period (Table 2, Fig. 5B). Birds fed the medium-quality diet

assimilated 9.7% more OM than birds on the low-quality diet (P<0.01,

Table 3). Birds fed the high-quality diet assimilated 13.9% more OM

than birds on the low-quality diet (P<0.01, Tables 2 and 3). No

significant differences were found between medium- and high-quality

diets (Table 3). Multiple comparisons of OM among diets yielded the

pattern of H=M>L (Fig. 5B) in contrast to the predicted H>M>L. No

significant pairwise temporal differences in AMC-OM were detected

within diets (Table 4).

Mean AMCs of nitrogen varied significantly among diets (P<0.01),

but not sampling periods (P=0.08, Table 2, Fig. 6A). No interactions

of diet and sampling periods on AMC-N were detected by ANOVA (P-0.55,

Table 2). When all sampling periods were combined (N=16), AMC-N was

15% higher in birds on the medium- than low-quality diet, 25% higher in

birds on the high- than low-quality diet, and 10% higher in birds on

50 -1

0 I I I
o 1 2 3 4 5

Sampling Period

----*--- Low
---*-- High


S--......4---- i

0 1 2 3 4 5
o 1 2 3 4 5

Sampling Period

Mean ( SE) assimilable mass coefficients for (A) nitrogen
(AMC-N) and (B) neutral detergent fiber (AMC-NDF) of adult
male Red-winged Blackbirds fed 1 of 3 diets. See Table 1
for diet contents. Four birds per sampling period were
used for estimates.



Figure 6.


high than medium diets (Tables 2 and 3). Multiple comparisons yielded

the pattern of AMC-N among diets of H>M>L (Fig. 6A) as was predicted.

Mean AMCs of neutral detergent fiber varied significantly among

diets (P<0.01), but not sampling periods (P-0.10, Table 2, Fig. 6B).

No interactions of diet and sampling periods were observed on AMC-NDF

(P=0.34, Table 2). In all sampling periods combined, birds eating the

high- and medium-quality diets had AMC-NDFs that were 27% to 30%

higher, respectively, than birds on the low-quality diet, with no

significant differences between medium- and high diets (Tables 2 and

3). Multiple comparisons among diets yielded the pattern of AMC-NDF of

H=M>L (Fig. 6B) in contrast to the predicted H>M>L.

Gut Anatomy

Main experiment. Mean gizzard mass differed significantly with

diet (P<0.01) and sampling period (P=0.05, Table 2). In all 4 sampling

periods combined, gizzard mass was 20% larger in birds on the low- than

high-quality diet, 17% larger in birds on the medium than high diets,

but did not differ between low- and medium-quality diets (Tables 2 and

3). Multiple comparisons yielded the pattern of gizzard mass among

diets of L=M>H, in contrast to the expected L>M>H. Increased gizzard

mass may have resulted from development of the muscles surrounding the

gizzard due to increased grinding action caused by greater intake in

birds on the low- and medium-quality diets when compared with those on

the high-quality diet.

Small intestine length varied with diet (P=0.02), but not sampling

period (Table 2). There was no interaction of diet and sampling period

on SIL. Birds fed the medium-quality diet had SIL that were 9% longer

than those on the high-quality diet (Tables 2 and 3).

Within diets, there were no relationships of MECs nor AMCs with

SIL (all P>0.10). Irrespective of diet, MECs and AMCs also were not

correlated with SIL (all P>0.12). Lack of a relationship of

digestibilities (MECs and AMCs) with small intestine length during the

first through fourth sampling periods suggests that this component of

gut volume may be of little relative importance to digestion and

absorption of energy, OM, N, and NDF in the short term. Other

mechanisms, such as enzyme induction or microscopic structure of the

absorptive surface may be more important than SIL in affecting short-

term digestive performance.

Length of cecum did not vary with diet or sampling period in the

full model 2-way ANOVA (Table 2), suggesting that gross morphological

adaptation to diets of varying qualities did not occur during the


Large intestine length was not measured in birds tested in the

diet quality experiment because samples of small intestine mucosa were

taken for a separate study of variation in enzyme activities with

variation in diet (Brugger and Martinez del Rio, unpubl. data). This

procedure required rapid removal of the small intestine, which was

accomplished by cutting the large intestine, rendering the large

intestine unmeasurable.

End-of-trial. Measures of intake and gut organ sizes, but not

digestive performance, were made with 18 birds in a fifth sampling

period. Measures of intake and gross gut morphology did not differ

between the fourth and fifth sampling groups (sacrificed on days 37 and

40) within diets; hence, they were combined as an end-of-trial group

(Table 5). Significant end-of-trial differences were found among diets

in body mass (P=0.04), intake (P<0.01), gizzard mass (P<0.01), and SIL

(P-0.03). An allometric relationship was found for gizzard mass.

Thus, the mean values were adjusted for body mass. Birds on the low-

quality diet had significantly larger body mass (P<0.02), but not

greater intake or larger gut organ sizes than birds on the medium-

quality diet. Birds on the low-quality diet had significantly greater

body mass, intake, gizzard mass, and longer SIL than those on the high-

quality diet (all P<0.05). Birds on the medium diet had similar body

mass and longer SIL than those on the high diet (each P50.03).

Within diets in the end-of-trial group, SIL was not correlated

with dry matter intake (all P>0.3). Additionally, irrespective of

diet, SIL was not related to intake (N-30). However, volumetric intake

and SIL were related. The relationship is described by the linear


SIL = 188 + 3.0 (Volumetric intake), r2 = 0.15, P<0.04. (14)

The presence of a direct relationship of SIL and volumetric intake in

the end-of-trial group, but not in preceding sampling periods, suggests

that small intestine length, and therefore gut volume, may be adjusted

as a long-term response to increased volume of feeding. The adaptation

of SIL to intake required more than 1 month in adult male Red-winged


Table 5. Mean (SE) measures of intake and gut anatomy for the end-of-
trial group, which comprised birds of the fourth and fifth sampling
periods (N=10 per diet). Results of 1-way ANOVA are presented (F, P).
Abbreviations are as in Table 2. Means for gizzard mass are adjusted
for covariance with body mass. Letters above means represent
significant differences as determined by multiple comparisons.

Dependent Diet Ouality
variable Low Medium High F2,27 P

Body mass (g) 59.4A (1.2) 53.6B (1.8) 56.5B (1.5) 3.5 0.04

Intake (g) 14.5A (0.3) 13.5A (0.3) 10.1B (0.4) 48.0 <0.01

Gizzard mass (mg) 1,338A (53) 1,287A (77) 1,023B (47) 7.7 <0.01

SIL (mm) 211.1A (5.0) 214.5A (4.3) 201.1B (4.1) 3.8 0.03

Cecum (mm) 4.7 (0.3) 4.5 (0.4) 5.0 (0.2) 0.7 0.51

There were significant differences among diets in 3 histological

measures in the small intestine (Table 6). Birds that were fed the

bulky medium-quality diet had deeper basement membrane (6%), longer

villi (17%), and larger diameter of the small intestine when compared

with those on the high-quality diet (Table 6). No significant

differences were detected between birds on the low- and high-quality

diets (each P>0.4). These results demonstrate the effect of sawdust

diluent in the diet on microstructure of the small intestine.

Table 6. Mean (SE) depth of basement membrane, depth of crypts of
Lieberkuhn, length of villi, diameter of lumen, and diameter of the
intestine for 4 birds per diet sacrificed after 40 days of exposure to
the diet. Results of a nested 2-way ANOVA (subjects, each with 5
repeated measures, nested within diets) for the effects of diet are

Diet Quality

Parameter Low Medium High F P

Basement (pm) 73 ( 3) 83 ( 5) 68 ( 3) 4.9 0.01

Crypts (pUn) 319 ( 17) 303 ( 9) 308 ( 20) 1.6 0.20

Villi (Pm) 869 ( 31) 938 ( 27) 802 ( 78) 46.6 <0.01

Lumen (uim) 1,105 (175) 1,089 ( 87) 1,144 ( 74) 1.8 0.17

Diameter (um) 3,621 (101) 3,743 (112) 3,527 (110) 12.5 <0.01

Experiment II: Season

The series of 4 feeding trials was conducted during a warm year in

Florida. Maximum and minimum air temperatures among months of the

trials are shown in Fig. 7. Tests were performed with 48 birds. Of

these, 43 birds were in energy balance and positive nitrogen balance

(Table 7). No allometric effects on digestive or anatomical responses

were detected.

Intake. Defecation. Metabolizable Energy Intake, and Transit

Mean daily dry matter intake, and defecation varied significantly

among seasons (Table 7). Intake was 14% higher and defecation was 29%

higher in February than August (both P<0.01, Tables 7 and 8). Among

all trials combined, defecation was related to intake by the equation

Defecation = 0.38*(Intake) + 0.13, r2-0.61, P<0.05. (15)

The relationship was not significantly different from equation 8 (page

49) for birds fed Purina Layena as a low-quality diet.

Metabolizable energy intake per bird per day was 17% higher in

February than August (P-0.04), but did not differ between May and

August (Table 8), suggesting that metabolic demand was highest in

February. Energy content of the feces did not vary among seasons

(Table 7), suggesting that there was not selective passage of high

energy materials among seasons.



. 20-
10 -



- I I I
0 5 10 15 20
Day of Feeding Trial


0 5 10 15 20
Day of Feeding Trial

I I I1
0 5 10 15 20
Day of Feeding Trial






I I I *

0 5 10 15 20
Day of Feeding Trial

Figure 7. Minimum (closed circles) and maximum (open circles) air
temperatures (oC) recorded in the covered aviary during
feeding trials conducted in (A) May, (B) August, and
(C) November 1988, and (D) February 1989.

Table 7. Results of 1-way ANOVA for feeding trials conducted during
May, August, and November 1988, and February 1989 with adult male Red-
winged Blackbirds. Means ( SE), sample sizes (N), F-ratio, and
probability of its deviation from 1 are given. Abbreviations are as in
Table 2. Mean (SE) and sample size (/N) for estimates of transit time

are provided for 3 of

4 feeding trials.

Feeding Trial



F3,39 P

Body mass(g)


Intake (g/d)


MEI (kJ/d)

FE (kJ/g)

Transit (min)

MEC (%)

AMC-OM (%)

AMC-N (%)


mass (-g)

SIL (-=-)

Cecum (mm)

LIL (mm)

56.7. (0.7)

302.0 (9.0)

10.9 (0.3)







67.3 (0.8)

62.0 (1.3)

34.2 (1.4)

33.8 (1.5)









55.4 (0.5)

287.0 (8.0)

10.4 (0.2)

























56.2 (0.7)















( 11)














56.6 (0.1) 0.54 0.65
































































Table 8. Unadjusted results of t-tests to reveal differences between
means for variables for which significant 1-way ANOVAs were reported in
Table 7. Comparisons were performed for values from August with those
of February and May, only, to conserve power of the tests. Results are
significant among 2 paired comparisons if P 5 0.025, following
Bonferonni's adjustment (a/k or 0.05/2). The value <0.01 indicates
numbers >0.00 and <0.01, and the value <0.02 indicates numbers >0.01
and <0.02. Abbreviations are as in Table 2.

Comparisons Between Months

Aug and May Aug and Feb
Variable t P t P

Intake (g/d) 1.18 0.25 4.24 <0.01

Defecation (g/d) 2.65 <0.02 6.34 <0.01

MEI (kJ/d) 0.29 0.77 2.31 0.04

MEC (%) 3.73 <0.01 3.56 <0.01

AMC-OM (%) 4.60 <0.01 3.68 <0.01

AMC-N (%) 3.25 <0.01 3.42 <0.01

LIL (mm) 2.14 0.05 3.41 <0.01

Mean transit times, as measured by the blue dyed food method did not

differ significantly among 3 seasons (Table 7). No measures of transit

were made during the May trials because no birds were observed

consuming the dyed food.


Digestibility of energy, as measured by MEC, varied significantly

among seasons (Table 7). The highest mean apparent MEC of 71% was

observed during August, the lowest of 66.9% in February (P<0.01, Table

8). For all 43 birds combined, there was no correlation between intake

and MEC. However, an analysis of covariance preliminary model showed a

significant effect of the interaction of season and intake (the

covariate) on MEC (F-5.52, P<0.01), indicating that the MEC/intake

slopes were not equivalent among seasons (Fig. 8). In May and August,

the slopes of the regressions of MEC on intake were not significantly

different from 0, suggesting that efficiencies were static with varying

intake. Yet, in November and February, the slopes were significantly

positive, suggesting increased efficiencies with increased intake.

Apparent AMCs of organic matter and nitrogen varied significantly

among seasons (Table 7). Values from August were 5.5% and 8% higher,

respectively, than those from February (both P<0.01, Table 8). Values

from the August trial were also higher than the May trial by 7% for OM

and nitrogen (both P<0.01). The ANCOVA preliminary model, performed

for AMC-OM and AMC-N, showed a significant effect of the interaction of

season and intake on AMCs (both P<0.01), indicating nonequivalence of

slopes among seasons for each variable. Seasonal plots of AMCs on

y = 81.65 0.43x

r=0.48, P=0.13

0 0 *
0 ^"T 0 U

I Ili
9 10 11 12 13
Intake (g/d)

y = 48.78 + 0.62x

r 0.64, P < 0.05

9? S


8 9 10 11 12 13
Intake (g/d)

r = 0.56, P =0.09


8 9 10 11 12
Intake (g/d)

y 42.96 + 0.64x

r 0.64, P < 0.03


10 11 12 13 14 15

Intake (g/d)

Regressions of apparent metabolizable energy coefficients
(MEC) on intake for adult male Red-winged Blackbirds fed a
controlled diet during four seasonal feeding trials
conducted in (A) May, (B) August, and (C) November 1988,
and (D) February 1989. Pearson's correlation coefficient
(r) is given for each regression.

Figure 8.

y = 83.14 0.38x

intake revealed similar seasonal patterns as observed in the MEC/intake

plots (Fig. 8), suggesting an increase in AMCs with increased intake in

cold months, but no relationship of AMCs and intake in warm months. No

differences among seasons were found for AMC-NDF (Table 7).

Gut Anatomy

Only 1 measure of gut size varied significantly with season:

length of large intestine (Table 7). The mean length of the large

intestine of birds in the August trials was 28% greater than that in

birds of the February trials (P<0.01) and 15% greater than in May

(P<0.05). However, with Bonferonni's adjustment, only the August-

February comparison is significant. The large intestine of birds is

involved in water resorption and electrolyte balance. Birds may suffer

greater water loss in late summer due to heat stress or molt. Thus an

increased length of large intestine may be related to water

conservation in late summer. Alternatively, LIL may be inversely

related to intake, by an unknown mechanism. There was no relationship

of SIL to intake or MEC within or irrespective of season.

Experiment IIIT Photoperiod

Complete measures were made for 12 birds. All birds were in

energy balance and positive nitrogen balance (Table 9). No allometric

effects on digestive or anatomical responses were detected.

Intake. Defecation. Metabolizable Energy Intake. and Transit

There were no differences between daylength treatments in mean

daily dry matter intake, dry mass of feces, transit time, energy

content of feces, or daily MEI per bird (Table 9). These data suggest

that activity patterns, energetic demands, and transit do not differ

because of photoperiod, in the range of daylengths tested.


Apparent MECs did not differ between photoperiod treatments

(P>0.9). Data from the 2 groups were then combined. There was no

relationship between MEC and intake (P-0.52). There were no

differences in AMCs of organic matter, nitrogen, or fiber in birds held

under long or short light cycles (Table 9). These results also suggest

that a 6 h difference in daylength did not affect metabolic demand or

digestive performance in captive redwings held in the thermoneutral


Body Mass. Gut Anatomy. and Reproductive Condition

Within a light treatment, birds killed before the 3-day digestion

trial had similar measures of body mass and gut anatomy as birds that

completed the digestion trials (all P>0.5), suggesting that

disturbances of the digestion trial did not bias measures of gut

anatomy. There were no differences in measures of body mass or gut

Table 9. Results of photoperiod experiments conducted during January
1988 with 12 adult male Red-winged Blackbirds held in environmental
chambers at 20 oC and light cycles of either 9L:15D or 15L:9D. Diet
composition is reported in Table 1. Sample size (N), mean (SE),
Student's t, and probability are given. Abbreviations are as in Table


Short Long

9L:15D 15L:9D

Parameter (N=6) (N-6) t P

Body Mass (g)

balance (mg)

Intake (g)

Defecation (g)

Transit (min)

FE (kJ/g)

MEI (kJ/d)

MEC (%)

AMC-OM (%)

AMC-N (%)


Gizzard Wall (mm)

SIL (mnm)

Cecum (mm)

LIL (rm)

Testes (mg)


54.0 (2.6)

















( 19)



( 13)













56.4 (1.4)

















( 12)



( 12)













0.77 0.45

































organ sizes between photoperiod treatments (Table 9). In the combined

samples of long- and short-day birds (N=12), there were no

relationships of MECs nor AMCs to SIL (all P20.3).

Birds in the long-day cycle had larger testes and higher blood

testosterone concentrations (up to 30x) than those on the short-day

light cycle (Table 9). Dry mass of the testes was similar to that of

wild birds in breeding condition (Payne 1969). However, the mean

testosterone concentration in the captive birds was only 20% that of

wild males in breeding condition (Harding and Follett 1979). There was

no significant relationship between blood testosterone and any of the

digestion variables, suggesting that the limited hormonal changes

associated with photoperiod-induced breeding condition in captive male

redwings had no effect on gut anatomy or digestive performance.

Experiment IV: Temperature

Complete measures were made for 12 birds. All birds were in

energy balance and positive nitrogen balance (Table 10). No allometric

effects on digestive or anatomical responses were detected.

Intake. Defecation. Metabolizable Energy Intake. and Transit

Intake differed significantly between temperature treatments

(P<0.01, Table 10). Mean daily dry mass of feces also differed between

treatments (P<0.01). Birds held at 7 oC had a mean daily dry matter

Table 10. Results of temperature experiment conducted during November
1988 with 12 adult male Red-winged Blackbirds held in environmental
chambers on a light cycle of 12L:12D at either 7 oC or 20 oC. Diet
composition is given in Table 1. Sample size (N), mean (SE),
Student's t, and probability are given. Abbreviations are as in Table


7 OC 20 C

Parameter (N=6) (N-6) t P

Body mass (g) 56.7 (1.3) 55.0 (1.3) 0.89 0.39

balance (mg) 52.0 (17.0) 90.0 (7.0) 3.98 <0.01

Intake (g) 8.4 (0.5) 6.5 (0.2) 3.29 <0.01

Defecation (g) 3.4 (0.2) 1.8 (0.1) 5.79 <0.01

Transit (min) 46.3 (8.6) 40.6 (6.9) 0.51 0.63

FE (kJ/g) 13.4 (0.1) 13.8 (0.1) 2.18 <0.06

MEI (kJ/d) 94.2 (6.2) 85.4 (3.1) 1.24 0.24

MEC (%) 66.7 (1.6) 77.3 (1.5) 4.81 <0.01

AMC-OM (%) 63.0 (2.0) 74.5 (1.8) 4.32 <0.01

AMC-N (%) 19.8 (6.2) 47.5 (3.4) 3.92 <0.01

AMC-NDF (%) 22.6 (4.0) 49.3 (3.8) 4.87 <0.01

Gizzard mass (mg) 1,045.1 ( 63) 842.5 ( 38) 2.72 0.02

SIL (mm) 191.6 (3.0) 197.0 (2.3) 1.38 0.19

Cecum (mm) 4.0 (0.2) 4.0 (0.2) 0.00 1.00

LIL (mm) 15.5 (0.9) 14.8 (0.6) 0.57 0.57

intake of 8.4 g and defecation of 3.4 g compared with a mean intake of

6.5 g and defecation of 1.8 g for those held at 20 OC (Table 10). Mean

transit time (P=0.63) and mean energy content of the feces (P<0.06) did

not differ significantly with temperature (Table 10). Relative

differences in intake and MEC between treatments yielded no differences

in mean daily metabolizable energy intake of approximately 90 kJ per

bird (P=0.24).


There was a significant difference in apparent MECs between

temperature treatments (P<0.01) with birds at 20 OC showing a 10%

increase in energy efficiencies over birds at 7 OC (Table 10). There

was no relationship between MEC and intake in either temperature group

alone (both P>0.6). However, irrespective of temperature there was a

trend of inverse relationship between MEC and intake (P-0.06). The

AMCs of OM, N and NDF differed with temperature, with birds in the 20

oC chambers approximately 10% more efficient at assimilating OM

(P<0.01), 30% more efficient at assimilating N (P<0.01), and 25% more

efficient at assimilating fiber (P<0.01, Table 10).

Body Mass and Gut Anatomy

Within a temperature treatment, birds killed before the digestion

trial had similar body mass and gut organ sizes as those included in

the trial (all P>0.05), suggesting that the digestion trial had no

effect on the gut anatomy of the test birds. Only gizzard mass of

birds included in the digestion trials differed between temperature

treatments, with birds in the 7 oC chamber having a gizzard about 20%

heavier than those in the 20 oC chamber (Table 10). Small intestine

length did not differ between treatments. Irrespective of temperature

treatments, SIL was inversely related to intake, as described by the


SIL= 220 3.471 (Intake), r2 = 0.67, P<0.02. (16)

The relationship of SIL and intake was in conflict with that observed

in Experiment I (equation 14, page 58). There was no relationship of

MEC to SIL (P>0.4) for birds of Experiment IV.


I conducted 4 feeding experiments with captive adult male Red-

winged Blackbirds to identify digestive and anatomical responses to 3

external variables, diet, photoperiod, and temperature, and associated

responses to internal changes in metabolic demand and reproductive

condition. Digestive responses to exogenous and endogenous

fluctuations may enable Red-winged Blackbirds to process a broad diet

throughout the year, thus affecting nutrient balance in the bird. Four

general responses were examined: changes in intake, digestibilities,

sizes of gastrointestinal organs, and retention times.

Intake and Digestibilities

Intake and digestibilities interact to set the level of net energy

and nutrient uptake by an animal. Intake is recognized as the major

variable affecting digestibility of a diet among domestic animals (Van

Soest 1982, Robbins 1983). This is because retention time is assumed

to increase with decreased intake, such that digesta remain in contact

with the mucosa for longer periods, and hydrolysis and absorption


Many factors affect intake and digestibilities. Intake is

regarded as a parameter of food quality and is influenced by metabolic

demand, body size, age, sex, nutritional status of the animal, and gut

fill. Digestibilities generally increase with trophic level (Koslowski

1968) irrespective of taxonomic class (Woods 1982). Within taxa,

digestibilities also vary according to type of food consumed (Castro et

al. 1989, Karasov in press).

Environmental conditions of feeding trials also affect measures of

intake and digestibilities. In fact, direct comparisons among results

of the experiments for intake and digestibilities are difficult to make

because the actual conditions of each feeding experiment differed

greatly from the others, despite the attempt to standardize diets and

control daylength and temperature. Basal metabolic rates, insulation,

and activity patterns probably differed among the 4 experiments,

yielding differences in intakes and digestibilities for similar

temperature and photoperiod conditions. Birds tested in January

(Experiment III) and February (Experiment II) probably had the highest

SMR because of seasonal fluctuation in thermoregulatory demands

(Brenner 1966, Kendeigh 1949, 1972). Birds tested in November

(Experiments II and IV) had the greatest insulative cover because molt

is complete by October. Birds housed in the aviary (Experiments I and

II) were subject to relatively high disturbances because it is large,

outdoors, and was used to hold other birds. Birds tested in the

environmental chambers (Experiments III and IV) experienced less

disturbance because of its small size and tight insulation. Thus,

birds tested in the aviary when it was at its fullest (Experiment I)

probably had the highest costs of activity when compared with others.

This is reflected in the high measures of MEI for the warm temperatures

at which Experiment I was conducted. Despite these difficulties in

comparing results of the 4 experiments, the responses that were

elicited within experiments show relative directional changes that

indicate patterns in digestive responses by redwings. Thus, I will use

proportional changes in intake and efficiencies as a basis for


Exogenous Factors

Diet. Among the 4 experiments, the largest ranges of intake and

digestibilities of energy, organic matter, nitrogen, and fiber by adult

male Red-winged Blackbirds were obtained by varying quality of the

diet. Mean intake varied 30%, energy and OM digestibilities varied up

to 15%, and nitrogen and NDF efficiencies varied up to 35% among diets.

The composition of the high-quality diet resulted in low intake, but

similar MEIs when compared with redwings on the other diets. These

results are similar to those found for domestic animals (Van Soest

1982), as well as for many wild birds (Williams and Hansell 1981, Moss

1983, Levey and Karasov 1989, Karasov in press).

Stabilization of intake by birds on the high quality-diet took

more than 2 weeks, as evidenced by the prominent decrease in mean

intake by birds in the third sampling period. It is possible that,

because of the high energy and protein contents of the high-quality

diet, acclimation took longer in these birds than in birds fed the 2

lower quality diets.

Clearly the physical and chemical structures of food are the most

important factors that determine intake and digestibilities because the

physical and chemical processes in an animal set the limits to

consumption and digestion. The physical structure of foods may limit

intake if the energy-density of the food is very low (Kenward and Sibly

1977), or may limit access of digestive enzymes to the cell contents if

an animal does not have the ability to break open the cells. For

example, an animal without teeth, fermentation chambers, symbiotic

microflora, or acid secretions will have low digestibilities of fiber

because the structural carbohydrates limit access to nutrients

contained in the cell contents and the cell wall (Van Soest 1982).

Additionally, the chemical composition of a diet directly affects

net gain of energy and nutrients by means of setting limits to the

biochemical reactions in the gut. Hydrolysis and absorption are

dependent on matching of the enzyme or carrier to its substrate as well

as on temperature and pH constraints. An animal without the

biochemical means to hydrolize food molecules, for example a European

starling without sucrase (Martinez del Rio and Stevens 1989), cannot

obtain the energy contained within specific food compounds, such as

sucrose. Thus food chemistry is of primary importance to predicting

the rate and extent of energy and nutrient gain.

Season. Intake varied 17% and digestibilities varied up to 8%

among seasons, with a trend of the highest mean intake and lowest mean

efficiencies in winter. However, the relationship of individual MECs

(and AMCs) to intake was not consistent in redwings among seasonal

tests. During feeding trials conducted in warm weather, no

relationship between MEC and intake was found, whereas in cold weather,

a significant increase in MEC occurred with increased intake. Both

results are contrary to those expected.

This unexpected relationship may reflect the narrow range of

experimental conditions to which the redwings were subjected. I made

my MEC determinations over the natural range of intakes by birds

feeding ad libitum (8.2 to 15 g/d), which is less than those used by

Sibbald (1975) for chickens (5 to 90 g/d). Thus, the 2-fold difference

in feeding rate for caged Red-winged Blackbirds throughout the year may

not have been enough to elucidate a consistent pattern in relationship

between intake and MECs.

Alternatively, the results may reflect individual variation in

feeding habits or health of the birds. Healthy birds may eat well and

digest food efficiently, while birds that have low-level infections may

eat less food and digest the diets poorly. The disparity may be

exaggerated in cooler months when respiratory or other infections might

affect the birds, resulting in an apparent direct relationship of

intake and digestibilities.

Photo~eriod. No variation in intake or digestibilities were

attributed to daylength alone in the range of photoperiods tested.

Previous studies with redwings and other passerines reported

conflicting results concerning the relationship of photoperiod with

intake and digestibilities. For example, when photoperiod was

increased from 12L to 14L at a temperature in the range of 21 oC to

25 C for male and female redwings, neither intake nor MECs increased

(Brenner 1966). In another study, increasing photoperiod from 8L to

18L at 20 OC resulted in a linear increase in intake, with no change in

MEC for adult male redwings (Brenner and Hayes 1985). A direct

relationship of photoperiod and intake, with an indirect relationship

of photoperiod and MEC has been shown for House Sparrows (Passer

domesticus, Kendeigh 1949, Davis 1955), Tree Sparrows (Spizella

arborea, West 1960), Field Sparrows (Spizella pusilla, Olson and

Kendeigh 1980), and Dickcissels (Siz americana, Zimmerman 1965). On

the other hand, lack of a relationship among photoperiod, intake and

MEC has been documented for House Sparrows, White-throated Sparrows

(Zonotrichia albicollia, Siebert 1949), and Redpolls (Brooks 1968).

The studies were conducted at all times of the year, with various

photoperiod regimes, thus nonstandardization may influence the results.

However, lack of agreement among studies suggests photoperiod-specific

and possibly taxon-specific digestive responses to the external

stimulus of photoperiod.

Temperature. Intake varied 30%, digestibilities of energy and OM

varied 10%, and digestibilities of N and NDF varied almost 30% between

temperature treatments. The ranges in intake and digestibilities for

birds at 2 temperatures represent the second greatest ranges among the

4 experiments. Results of the diet and temperature experiments

demonstrate that the influence on digestive responses of a decrease in

temperature from 20 oC to 7 OC are less than those of 2.5 kJ/g and 2.5%

change in energy density and nitrogen, respectively, in determining net

gain of energy and nutrients.

The decrease in digestibilities with declining temperature may be

intake-related, because intake was higher in birds held at the low

temperature when compared with those at 20 oC. However, the decrease in

MEC was not proportional to the decrease in AMC-N or AMC-NDF between

temperatures. The discrepancy could be a consequence of temperature-

dependent functions or methodology.

In the thermoneutral zone (20-40 OC), body temperature of birds is

regulated primarily by changing the effectiveness of the external body

insulation (Kendeigh et al. 1977). In low temperatures, metabolic heat

is used to regulate body temperature. During cold conditions, energy

might be diverted from cellular work in the digestive tract to heat

production for thermoregulation. Thus, rates of secretions, or

hydrolysis and absorption may decrease with ambient temperature,

resulting in decreased digestibilities of specific materials. For

example, reduction in body temperature by 3 oC over a decline in

ambient from 40 oC to 0 oC (Lustick 1975) may have direct Q10 effects

on enzyme kinetics. Such changes in digestive efficiencies with

changes in temperature have been documented in a variety of birds. The

changes were rarely linear and often show peaks at specific

temperatures (Zimmerman 1965, Brooks 1968, Willson and Harmeson 1973).

Low air temperature of Experiment IV was associated with the

lowest value of AMC-N obtained for any of the experiments. Low AMC-N

was also reported for Tree Sparrow held at -14 oC (Robbins 1981). The

low AMC-N could be a result of methodology. Nitrogen composition of

urine and stability of the compounds is temperature-dependent. Urine

of birds contains several nitrogenous components: uric acid, urea,

ammonia, purines, creatine, and free amino acids. The components vary

in relative proportions of the total nitrogen depending on level of

feeding, ambient temperature, and amino acid balance. High temperature

(Edwards and Wilson 1954), starvation (Sykes 1971), and amino acid

imbalance (Teekell et al. 1968) decrease the proportion of uric acid

and increase the proportion of ammonia in the urine of chickens. If

similar responses occur in redwings, then falsely high estimates of

assimilation efficiencies of nitrogen could occur at high ambient

temperatures. The relatively large proportion of nitrogen excreted as

ammonia would vaporize during the 24-h collection periods or when feces

were dried for analysis. Thus the interpretation of the assimilable

mass coefficient for nitrogen would be incorrect in high temperatures.

Nitrogen would not have been assimilated by the bird; instead it would

have been excreted and lost to the environment.

If temperature-dependent functions or methodology resulted in

biased nitrogen estimates, then a consistent bias would be expected

among the experiments. All birds tested at low temperatures would show

reduced AMC-N. This was not the case. Birds tested in winter in

Experiment II had similar AMC-N as those in summer, not markedly

reduced values. Additionally, if temperature-dependent production of

nitrogenous compounds were occurring in redwings, a bias would be

expressed in the values of nitrogen balance. Birds tested at high

temperatures would show very high nitrogen balance, if ammonia nitrogen

evaporated. They did not. Alternative explanations are needed for the

observation of reduced AMC-N at low temperatures.

Endogenous Factors

Reproductive condition. No variation in intake or digestibilities

were attributed to daylength alone or to the associated changes in

breeding condition of birds on the long-day cycle. Low concentrations

of testosterone were elicited, which may have biased any potential

responses to endocrine change. However, the birds with the very

highest testosterone levels showed no change in intake or

digestibility. These results suggest that there is not a confounding

effect of reproductive status on digestive responses.

Fiber Digestion

The AMC-NDF obtained in these experiments were unexpectedly high

and deserve special attention. They reflect the digestibility of the

structural components of the diet (i.e., cellulose, hemicellulose, and

lignin in the cell walls). Vertebrates lack the enzymes to digest the

A-linkages of NDF carbohydrates, but those that harbor bacteria and

fungi capable of hydrolizing the bonds may utilize the energy contained

in cell walls. Acid hydrolysis of structural carbohydrates also may

contribute to fiber digestion (Parra 1978).

Digestibilities of NDF are inversely related to the lignin

concentration of the acid detergent fiber (Parra 1978). Wild ruminants

that consume a diet with 15% to 30% lignin in the ADF (the range

offered to redwings in these feeding experiments ITable 1]) exhibit NDF

digestibilities of 30% to 55%. Data from redwings show NDF

digestibilities that ranged from 20% in Experiment IV to 70% in

Experiment I.

The high digestibilities of NDF by redwings suggest that they can

digest a portion of the structural carbohydrates of the cell walls.

Where and how do redwings digest fiber? If fiber is digested, are the

products then absorbed? Fiber digestion has been reported to occur in

4 locations by 2 methods in birds: foregut fermentation (e.g., Hoatzin,

Opisthocomus hoazin, Grajal et al. 1989); distal ileum fermentation

(e.g., Emu, Domaius novaehollandiae, Herd and Dawson 1984); cecal

fermentation (e.g., Ptarmigan, Lagoaus spp., Gasaway 1976); and acid

degradation of fiber in the gizzard, with potential intestinal

absorption of soluble carbohydrates and cecal fermentation of selected

portions of the digesta (e.g., Australian Wood Duck, Chenonetta iubata,

Dawson et al. 1989).

The fourth method of fiber digestion is the most likely in

redwings because of their simple gut morphology and rapid transit

times. The foregut and hindgut of Red-winged Blackbirds are not

enlarged, suggesting little potential for storage of fibrous portions

of the digest to allow fermentation. Long retention is typically

required to accomplish fermentation; however, throughput of digest is

rapid in redwings, potentially precluding fermentation. Fiber

digestion could occur in the gizzard and small intestine if acid of the

proventriculus and particle reduction by the gizzard are sufficient to

initiate acid hydrolysis of hemicelluloses (Dawson et al. 1989,

Buchsbaum et al. 1986). Reflux of fibrous materials in the small

intestine then might allow fibers to remain in the gut long enough for

complete hydrolysis to occur. It is possible that microbial

fermentation takes place in the ceca if selective flow of digesta to

the ceca occurs (McNab 1973, Gasaway 1976). But questions of whether

fiber digestion occurs and how the products of digestion might be

absorbed remain to be answered. Future investigations of cellulose and

hemicellulose digestion in redwings might focus on the role of the

proventriculus, gizzard, and the small intestine in hydrolysis and role

of lower portions of the small intestine, the ceca, and large intestine

in absorption.

Morphological Responses

Changes in size, shape, or form of gastrointestinal organs may

occur by means of simple stretching of the tissues, termed hypertrophy,

or increase in cell number, termed hyperplasia. Both occur in response

to increased intake (Johnson 1987). Methodology to distinguish between

the 2 relies on tissue culture techniques to measure DNA content or to

count cells. Relative differences in measures of redwing gut anatomy

between treatments will be discussed with respect to each mechanism.

Exoaenous factors

Diet. Several mechanisms promote growth of the gut. Data are

lacking for birds, but evidence from research with rodents suggests

that the contents of the gut may be responsible for shaping its

histology and growth (Goss 1978, Robinson et al. 1981). Although

simple stretching of the stomach from experimentally induced

hyperphagia was not sufficient to promote growth, increased nutrition

and absorption trigger gastric growth (Jervis and Levin 1966). In

addition, growth of the small intestine has been induced by

hyperphagia, being reversed by starvation (Fabry and Kukojovola 1960).

Growth of proximal portions of the small intestine was induced after

surgical resections and may be related to exposure to local nutrition

(Altmann and Leblond 1970).

Similar mechanisms may be found in birds and are suggested by the

results of these feeding trials as well as other experiments with

birds. Variation in gizzard mass was likely related to increased

levels of feeding. Birds fed diets that were energy-dilute and birds

kept at low temperature had relatively high intake and large gizzard

mass. The increase in gizzard mass probably resulted from development

of muscles surrounding the gizzard because of greater grinding action

with greater intake of diets with relatively high NDF contents. Simple

stretching would not produce change in mass of the gizzard. Similar

growth responses have been documented for gallinaceous birds (Leopold

1953, Savory and Gentle 1976a, 1976b), ducks (Miller 1975), and

passerines (Davis 1961, Ankney and Scott 1988).

There was a direct relationship of volumetric intake and SIL in

birds tested with 3 diets. The response required 5 weeks to occur. If

increased SIL was due to stretching of the gut tissue from increased

intake, the relationship should have been observed immediately after

diet switch in the first 3 sampling periods, which it was not. If

change in SIL was due to growth of the tissue, then a lag in response

would be expected such that cell accumulation would occur sufficiently

to produce measurable growth. Cell proliferation may begin within 3 to

4 days of a change in local nutrition or hormonal status of animals,

and accumulation of cells may produce measurable differences in SIL

after 7 to 10 days (Johnson 1987).

Direct responses of gut capacity to intake have been identified in

other birds and are presumably due to growth, not stretching, of the

tissue. Increased SIL from 27.5 cm to 33 cm was elicited in captive

European starlings after 14 days in response to an increase in intake

from 8 g/d to 40 g/d caused by diet dilution (Al-Joborae 1980).

Increases of 43% in SIL and 23% in combined ceca lengths were elicited

in Japanese quail in 21 days, in response to a 34% increase in

volumetric intake caused by diet dilution (Savory and Gentle 1976a,

1976b). Seasonal changes in gut capacity are also well known in wild

birds, with 5% to 30% differences in gizzard mass, SIL, and ceca

lengths occurring over 1 to 3 months (Moss 1974, Al-Joborae 1980, Al-

Dabbagh et al. 1987, Ankney and Scott 1988).

Season. The mean large intestine length of birds tested in August

was 28% greater than birds tested in February. Ambient temperature

likely played a causal role in the observed changes in LIL. The large

intestine is an important site of water, nitrogen, and electrolyte

conservation in birds (Skadhauge 1981). Urine can move from the cloaca

into the large intestine by antiperistalsis (Skadhauge 1976). It may

be that an increase in length of the large intestine increases

resorption of water in redwings, and is related to increased water

demands associated with thermoregulation in a warm climate.

Photoperiod. No relationships of intake and gut organ sizes were

identified with birds tested in Experiment III.

Temperature. Irrespective of temperature, intake was inversely

related to SIL in birds fed identical diets. The relationship is

directly opposite that found when birds were tested with 3 diets. The

temperature-related response may be related to nitrogen balance, such

that birds at low temperature catabolized protein in gastrointestinal

tissue for energy, whereas birds at high temperature did not. However,

birds at low temperature were in positive nitrogen balance, suggesting

that protein loss for energy did not occur.

Endogenous factors

There is hormonal influence over some aspects of gastrointestinal

growth. Nongastrointestinal hormones such as thyroxine and growth

hormone increase mucosal growth; gastrointestinal peptides such as

gastrin, cholecystokinin, secretin, and enteroglucagon elicit DNA

synthesis and cell growth in the intestine and pancreas (Al-Mukhtar et

al. 1981, Johnson 1987). Testosterone affects nontarget tissues in

mice, causing growth of the small intestine (Wright et al. 1972) and

possibly affecting digestion. Testosterone was correlated with

depressed growth of skeletal muscle in turkeys and chickens (Scanes


I looked for a relationship of testosterone levels and digestive

response in adult male Red-winged Blackbirds. Redwings in reproductive

condition showed no relationship of testosterone concentration and size

of the gut or digestibilities. However, the mean testosterone

concentration in the captive redwings was less than 20% that of wild

males (Harding and Follett 1979). The limited hormonal changes

associated with photoperiod-induced breeding condition in captive male

redwings might not have been sufficient to elicit morphological or

digestive responses, if they occur.

Predictions of Digestion Theory

Optimality models predict that gut volume and throughput time are

the two most significant parameters to maintaining flexible digestion

when an animal is faced with change in metabolic demands or diet

quality. Alteration of rates of hydrolysis and absorption has emerged

as a third variable of importance to an animal in regulating net gain

of energy and nutrients. Data collected in 4 feeding experiments

designed to examine the range of digestive and anatomical responses by

redwings to changes in diet, season, photoperiod, and temperature also

were used to evaluate predictions of digestion theory.

Gut Capacity

The first prediction I will address was identified in 2 optimality

models (Sibly 1981, Penry and Jumars 1986, 1987): gut volume should

increase when animals feed on diets of poor quality (i.e., low energy-

density) to increase the capacity of the "reaction tank." Variations

in sizes of the gizzard and small intestine of adult male Red-winged

Blackbirds were observed in experimental tests of 3 diets. Gizzard

mass was highest in birds fed low- and medium-quality diets. SIL

varied directly with diet-specific volumetric intake, but only after 5

wks of treatment. Villus length in the small intestine increased in

birds fed the voluminous medium-quality diet.

Gut capacity increased not only in response to variation in diet

quality, but also in response to fluctuation in temperature, as

observed in Experiment II and IV. Gizzard mass was highest in birds

held at low temperature. Length of the large intestine was greatest in

birds tested in summer.

These data support the general prediction of increased capacity of

the gut with decreased diet quality, and highlight the importance of

metabolic demand, created by low ambient temperature, as a contributing

factor. However, the prediction was nonspecific and implied a general

morphological response via growth of all organs. In reality, the

capacity, or volume, of the gut is probably of less importance to the

overall processes of digestion and absorption than are the functional

aspects of each organ. For example, the gizzard serves not only as a

site of chemical breakdown via acidification of the digesta, but also

as a site of physical reduction in sizes of food particles. Thus,

volumetric capacity of the gizzard has a direct bearing on total amount

of digesta that can be processed, but not necessarily the extent to

which it can be processed. Instead, increased muscular development of

the gizzard might be important for increasing the extent of food

processing by improving particle reduction as well as particle mixing,

thus serving to increase both the rate and extent of nutrient gain.

Such a response was evidenced by increased gizzard mass in redwings

when diet was poor or when energy demand was high.

Volume of the small intestine is probably of less functional

importance than is its "effective" surface area. The major sites of

enzymatic digestion and passive and active transport are in the brush

border of enterocytes that form the surface of the villus. Thus, an

increase in surface area of the small intestine might result in

proportional increases in the capacities for digestion and absorption.

Surface area of the small intestine may be increased by several means:

increasing its length or diameter, or increasing the lengths or density

of intestinal villi.

Surface area of the intestine of redwings varied via 2 mechanisms

in response to variation in diet quality: by a change in length of the

small intestine and by a change in length of villi. Increased SIL is

well documented in birds as a seasonal phenomenon (Moss 1974, Al-

Joborae 1980, Al-Dabbagh et al. 1987) as well as in response to dietary

manipulations (Savory and Gentle 1976a, 1976b, Moss 1983). However,

this is the first report for birds of adaptation by villi to diet.

Variation of villus length may have greater significance than SIL

to a bird faced with a need to increase the extent of digestion and

absorption. Assuming that the villus is a cylinder of constant radius,

and cylinder surface area is xlr2, a uniform 17% increase in lengths of

all intestinal villi (as observed in duodenal villi between the medium-

and high-quality diets) should represent a major increase in digestive

and absorptive surface area of 54%. Mean life-span of enterocytes is 6

days in rats, and rates of cell production may be altered by diet

(Williamson 1978). If enterocyte life span and cell production rates

of birds are similar, then there is a potential for fine adjustments in

surface area of the small intestine by means of regulating cell

production, and therefore villus length, over a matter of days.

Retention Time

The second prediction of optimal digestion also derives from 2

models (Sibly 1981, Penry and Jumars 1986, 1987): if intake is fixed,

and metabolic demand increases, an animal should increase retention

time to obtain increased extent of digestion. Although I did not fix

intake among seasonal feeding trials, the measures of voluntary intake

may be statistically controlled with ANCOVA after the feeding trials.

Metabolic demand, measured by MEI, varied among seasons and was

highest in February. Yet, no differences in transit times were

observed among seasons. Similar nonsignificant results were obtained

between temperature treatments where only metabolic demand differed.

Lack of differences in results of 3 experiments may be due in part

to the procedure of using dye markers and in part to the use of transit

time as a measure of retention. In other tests using dyes, rapid

appearance of colored feces indicated rapid passage of dye, but not

necessarily the food, through the gut (Hillerman et al. 1953).

Separate markers for the solid and liquid phases of the digesta might

have been more appropriate for use in redwings. Additionally, the

measures of mean and mode retention time might reveal different

patterns of food passage than transit time. Retention is a response

curve that describes the proportion of a meal appearing in the feces as

a function of time. Mean and mode retention times describe the

patterns of these excretion curves and are often used in comparative

studies because they provide mathematically derived values that enable

statistical testing (Warner 1981). Transit time of dyed food estimates

only the time of first appearance of digesta in the feces. Thus,

transit time identifies a minimum time of passage for digest, but does

not indicate the pattern of food passage in a bird. I assumed that

retention curves would be identical for birds on identical diets and

therefore reasoned that differences in overall retention would be

reflected in the simple measure of transit time.

There are few comparative studies with birds to evaluate the

observation of short-term changes in retention time in response to

variation in diet quality. Retention time in redwings may vary

inversely with food quality. Mean retention of unhulled millet seeds,

presumed to be difficult to digest because of the fibrous hulls, ranged

from 41 to 150 min, while that of Purina Startena, presumed to be more

easily digested because of commercial processing, was 16 to 66 min

(Matteson, unpubl. data). In poultry, retention time is directly

related to diet quality when the diet is diluted with fiber (Scott et

al. 1982). In hummingbirds, retention time appears directly related to

quality (-sugar concentration of the diet, Gass 1978, Martinez del Rio

and Karasov in press). In other vertebrates, short-term changes in

throughput have been documented in response to diet composition (Van

Soest 1982, Bjorndal 1989). Results of 3 feeding experiments with

redwings and published reports with other taxa do not support this

prediction of digestion theory. Further work is needed to address the

relationship of diet quality and retention.

Hydrolysis and Absorption

The third prediction comes from Sibly (1981): if there is no

possibility for change in size of the gut, then high demand should be

met with increased extent of digestion and absorption. Increased

extent of processing may be attained by increasing retention, enzyme

production, rates of enzyme reactions, number of transport carrier

sites, or rates of transport of molecules across the brush border

(Karasov and Diamond 1987). Thus Sibly's prediction might be met by

any one of these mechanisms.

Data from the 4 seasonal feeding trials present a case where diet

quality does not change and gizzard mass and SIL remain constant,

suggesting that the volume of the main portion of the digestive tract

does not change. Although the overall estimate of assimilation

efficiency, MEC, was lowest in the month with highest food demand

(February), total MEI was greatest at that time. Assuming that total

MEI reflects daily rates of digestion and absorption, then data from

seasonal feeding trials partially support the prediction that overall

food processing rates increase when demand increases. Full support of

the prediction is not possible because LIL varied among seasons, thus,

gut volume was not constant. The data further suggest that one or

several of the mechanisms listed above for increasing rates of

processing might be in operation seasonally in redwings.

Few comparative data exist for discussion of relative prevalence

of adjustable hydrolysis and absorption. Experimental studies with

poultry have identified materials such as metals or secondary compounds

in plants that inhibit enzyme and transporter activities, thus reducing