MORPHOMETRIC CHARACTERISTICS OF ESOPHAGUS AND INTESTINE IN TUFTED DUCKS AYTHYA FULIGULA WINTERING ON THE BALTIC COASTAL AREAS IN NORTH-WESTERN POLAND

Ewa Działa-Szczepańczyk¹, Iga Wesołowska^2
1 Department of Zoology and Apiculture, West Pomeranian University of Technology, Poland
² Department of Zoology, Agricultural University of Szczecin, Poland

ABSTRACT

The investigation object constituted the esophagus and intestine in 38 specimens of Aythya fuligula – 24 males (18 adult and 6 immature) and 14 females (7 and 7, respectively). The analysis comprised the length of the following parts of the alimentary canal, ie. esophagus, small intestine, paired ceca, large intestine, and the entire alimentary canal, regarding the sex, age, and  body size of the birds assessed by the four parameters, ie. body weight, body length, sternum length, and tarsometatarsal bone length.

Despite of the sexual dimorphism in the body size of Aythya fuligula, no differences of it were observed in the majority of the analyzed parameters of the alimentary tract. In the case of esophagus, however,  it was evidently longer in the drakes as compared to the females. The small intestine in the immature specimens, both males and females was longer than in the adult ones. Except the cecum length, the remaining parameters of the digestive tract were not related to the body size parameters in Aythya fuligula. The analysis of the correlations between the parameters of the digestive tract indicated a negative statistically significant relation between the esophagus and small intestine lengths as well as the entire length of the alimentary canal, and a positive relation between the small intestine length and the entire length of the alimentary canal.

Key words: Aythya fuligula, esophagus, intestine, morphometrics, morphology.

INTRODUCTION

Environmental diversification of the habitat of the birds and the consecutive ways of nourishment as well as the sorts of food, they feed on, constitute a source of a great variety in the structure of the digestive tract, both interspecific and intraspecific, between individual specimens. The intraspecific variability regarding the morphology of the digestive organs can also result from the genetic diversification of specimens in respect to sex, age, body size, state of health (eg. presence of  parasites in the alimentary canal), and physiology in the particular phase of life, eg. molt, migration, breeding, wintering periods.

Anseriformes considerably vary biologically and ecologically. They comprise herbivorous, carnivorous, as well as omnivorous species. The majority of the specimens of this order migrate, what results in seasonal alterations of their diet. Aythya fuligula belonging to the family: Anatidae, subfamily: Anatinae, tribe: Aythyini, genus: Aythya [8] is a migratory species included  in the omnivorous ducks. During winter it feeds mainly on vertebrates.

This work aims at the morphometric characteristics of the esophagus and the particular parts of the intestines (small intestine, paired ceca, and large intestine) in Aythya fuligula as well as the analysis of the results regarding the sex, age and the body parameters.

MATERIAL AND METHODS

The material of the study comprised the selected digestive organs (esophagus, small intestine, ceca, and large intestine) of 38 specimens of Aythya fuligula – 24 males (18 adult and 6 immature) and 14 females (7 adult and 7 immature) wintering on the Szczecin Bay and the Dąbie Lake in the years 1995-2006. The birds were collected from the fishing nets in which they had died while diving for fodder.

Had the sex and age been determined, the birds were weighed and the morphometric parameters of the body were assessed, including the body length, the sternum length, the tarsometatarsus length. The body weight was assessed exact to 1 g. The assessment of the linear parameters of the body was based on the method elaborated by Dziubin and Cooch [5]. The body length was measured with an elastic tape adherent to the dorsal side between the bill tip to the rump end, exact to 0.5 cm. The lengths of sternum and tarsometatarsus were measured with a caliper exact to 0.1 mm.

Morphometrics of the alimentary canal consisted in the length assessment of the following elements of the digestive tract, ie. esophagus (EL), small intestine (SIL), paired ceca (CL), and large intestine (RL). The organs were laid in line and measured exact to 0.1 cm according to the method programmed by Leopold [11]. The total length of the alimentary canal (TIL) equaled the sum of the lengths of esophagus, proventriculus, gizzard, small intestine, large intestine and cloaca. That parameter did not include the length of ceca.

The elaboration of the results comprised: arithmetic mean, standard deviation, coefficient of variability calculated for the particular parameters. Due to the t-Student test the statistical significance of the difference between males and females within the scope of average values of the analyzed parameters was assessed. No significance of difference between specimens within the age categories (in either groups of males and females) was assessed due to a scarce number of birds in those groups. Simultaneously with the investigation of the relations between measurements of the digestive organs and the body size as well as the relations between the parameters of the digestive organs, the coefficient of Pearson linear correlation (r) was assessed.

RESULTS

The basic characteristics of the statistic analysis are presented in Table 1. The average lengths of the successive parts of the alimentary canal in the investigated tufted ducks equal: esophagus – 145.78 mm, small intestine – 1745.52 mm, paired ceca – 252.58 mm, large intestine – 111.05 mm. The esophagus constituted 6.5% of the total length of alimentary canal, while the small intestine 78.4% and the large intestine 5%, respectively (Phot.1). The ceca were well developed, and their joint length proportion to the total intestine length amounted to 1 : 7.36.

The sexual structure of the investigated specimens of Aythya fuligula varied – the drakes constituted 63%. The sexual dimorphism in the body size was manifested by two measurements, ie. the body length and the sternum length, provided those values were higher in males as compared to females (Table 2). No sexual dimorphism in the lengths of the analyzed intestinal parts, nor the total length of the alimentary canal was indicated. However, the males differed significantly from the females in the length of esophagus, which was longer in males (Table 2).

Table 1. Absolute measurements of the body, esophagus and intestine in tufted duck Aythya fuligula; – mean, SD – standard deviation, CV – coefficient of variation, M – male, F – female, ad – adult individuals, im – immature individuals, BW – body weight, BL – body length, TL tarsus length, SL – sternum length, EL – oesophagus length,  SIL – small intestine length, CL – combined length of both caeca, RL – combined length of intestinum terminale and cloaca, TIL –  total length of digestive canal

Table 2. Differences in absolute body and oesophagus and intestine parameters between males and females of the tufted duck Aythya fuligula; – mean, SD – standard deviation, CV – coefficient of variation, M – males, F – females, t – value of t-Student's statistics , NS – statistically insignificant differences, p – level of significance, BW - body weight , BL – body length SL – sternum length, TL – tarsus length, EL – oesophagus length,  SIL – small intestine length, CL – combined length of both caeca, RL – combined length of intestinum terminale and cloaca, TIL – length of total digestive canal

The investigated birds differed in the age structure. The immature specimens constituted 34%. A difference in the length of the small intestine was observed between adult and immature specimens, in both groups of males and females (Table 1). It was longer in immature birds as compared to the adult ones. The statistic significance of the difference between age groups was not investigated, however.

The analysis of correlations between parameters of the body size and the alimentary canal indicated only one positive significant relation, ie. between the lengths of the sternum and the paired ceca. (Table 3).

The following relations between the average values of the measurements of the digestive organs were indicated, ie. a negative correlation between the lengths of esophagus and small intestine (r = – 0.53) and the total length of the alimentary canal (r = – 0.52) as well as a positive correlation between the length of small intestine and the total length of the alimentary canal (r = 0.97). For the remaining relations the value of the linear correlation coefficient proved to be statistically insignificant (Table 3).

DISCUSSION

The structure and the size proportions of the particular elements of the digestive tract in Aythya fuligula depends, similarly to other avian species, mainly on the sort of food. Kehoe and Ankney [9] examining five species of the genus Aythya indicated a close relationship between the diet of those birds and the parameters of ceca, the length of small intestine, the length and the weight of gizzard. Those researchers [9] noticed, that the species whose food contains more cellulose, have a longer small intestine and a heavier gizzard. Aythya fuligula is an omnivorous species. It feeds on plants and vertebrates in the summer. Whereas its winter food mainly consists of mollusks, snails, and crustaceans - mostly blue mussels and cockles while at sea, and zebra mussels on inland waters. At times Aythya fuligula feeds on small fish and frogs [2,8,13,17,19,31].

The variability between specimens within the analyzed parameters of the alimentary tract observed in the examined group of Aythya fuligula can originate in both the age and sex structure, and also in the differentiation of the body size, health (eg. degree of parasitic infection), and the kind and quantity of food. A close relation between the diet and the differentiation of organ sizes between specimens confirm the results of multiple experiments on wildfowl in captivity with various diets [10,14,15,16,24]. The research conducted on Mallard Anas platyrhynchos indicates a close relationship between the size of the digestive organs and the quality of the birds' food. According to Miller [15] there is a correlation between the contents of raw cellulose in the diet of Anas platyrhynchos and the size of its intestine. Kehoe et al. [10] indicated that the increase of the cellulose contents in the diet causes the increase of the sizes of the intestine and the stomach in that species.

The differentiation of the digestive tract parameters between the specimens of the given species can also result from the seasonal changes in the quantity and the sort of available food [6,7,12,20,32]. Lewin [12] observed a seasonal changeability of the intestine lengths in California Quail Lophortyx californicus brunnescens. The small intestine lengthened from 540 mm in the summer to 680 mm in the winter, while the ceca from 80 mm to 125 mm, respectively. The Aythya fuligula specimens in question were collected solely during the season of wintering. In this period the birds feed on a calorific and concentrated food (mollusks, snails, small fish, and frogs), different from that in the summer when the birds feed also on plants. The wintering time of those birds varied. They were collected between October and April, therefore their diet differed, what might have affected the assessed variability in the size of the digestive tract between specimens. The differentiation of the diet was noted in Aythya fuligula, wintering on the Swedish coast [17]. The birds mainly fed on snails of the family Hydrobiidae in March, while in September their food was dominated by mussels of the genus Cardium, and in December by the blue mussel Mytilus edulis.

The average total length of ceca in the examined group of Aythya fuligula amounted to 2067.76 mm. The ceca in those ducks are well developed, and their size depends on the diet. In certain birds the relationship between the size of ceca and the sort of food is clearly visible particularly in the herbivorous species, whose food contains indigestible cellulose [10,15,22].

The intraspecific variability in the size of the digestive organs can result from the differences in the body size of the individual specimens. The examined ducks varied in this respect – their body weight ranged between 820 g and 1230 g. The body size in winter can be determined by the quantity and sort of food, and henceforth affect the size of the digestive organs. Pulliainen [22] indicated in wintering Willow Grouse Lagopus lagopus, that lighter specimens (females and immature birds) had relatively longer small intestines and ceca as compared to heavier birds (males and adult specimens). Pulliainen [22] argued that lighter birds had to feed more than the heavier ones in order to survive in low temperatures. In the case when the food is less calorific and available in a limited quantity, the achievement of a necessary energy is possible due to the increase of its quantity what consequently results in the morphological changes in the alimentary canal [23].

Dimorphic variability in the values of the analyzed parameters of the alimentary canal connected with age were observed in the examined group of Aythya fuligula. They were particularly visible in the length of the small intestine. It was longer in the immature specimens in both male and female groups as compared to the adult ones. Due to a low number of age groups within each sex, no statistical significance of this variability was assessed. A similar size variability of the digestive organs in favor of the immature specimens was noted in the case of other avian species. A longer alimentary canal and particular parts of the intestine was noted in the immature males of  Velvet Scoter Melanitta fusca as compared to the adult ones [26]. Similarly, a longer small intestine was noted in the immature specimens of Mellanitta nigra of both sexes as compared to the  adult ones [4]. A similar phenomenon regarding both sexes in several species of Passeriformes was observed by Stevenson [25]. He indicated that the small intestine is relatively longer in immature birds as compared to the adult ones. 

No dimorphic differences dependent on sex were noted in the majority of the analyzed digestive organs in the group of Aythya fuligula. Bigger drakes, apart from the esophagus, did not differ in the lengths of the remaining parts of the alimentary canal from smaller ducks. Similar results were obtained in Common Scoter Mellanitta nigra [4]. The males and females did not differ in the lengths of the small intestine and ceca, however they did in the length of esophagus. The differences in the lengths of the digestive organs between males and females are not visible until  compared with the body measurements of those birds. The studies on the morphometrics of esophagus and intestines in Bean Goose Anser fabalis indicated that the indexes of the relative length of small intestine, as well as jejunum and ileum, calculated in relation to the body weight achieved higher values in females as compared to males, and that difference proved to be significant [28]. The differentiation in the sizes of the avian digestive organs between males and females can result from the dissimilarity of food preferences (quantity, sort and size of food) as well as a different frequency of feeding [3,18,20]. Such research was also conducted on Aythya fuligula. It proved that males and females differ considerably in the food preferences as to the species and size of mussels [2,3,18]. The research of Bengston [2] conducted on 72 specimens of Aythya fuligula during breeding indicated that the males ate a higher percentage of Chironomidae larva than females. Conversely, the females of that species ate twice as much mollusks of the genus Lymnaea as compared to the drakes. According to Draulans [3], who investigated the wintering Aythya fuligula, the males differed from the females in the food preferences regarding the size of Dreissena polymorpha. That experiment proved that, conversely to the drakes, the females ate mussels with shorter shells. Other observations on wintering Aythya fuligula indicated that the females preferred bigger shells in Corbicula japonica and smaller shells in Musculista senbousia, as compared to the males of that species [18].

The size differences of the avian digestive organs between males and females can result from various adjustment to the temporary changeable diet. The experiment of Barboza and Jorde [1] conducted in winter on Black Duck Anas rubripes reared in captivity proved that males and females subject to starvation periods of various frequency and length, responded differently with the morphological changes of digestive organs. The females developed an increase in the liver weight, intestine area, and the weight of the total digestive tract, while there were no such changes in drakes. The authors conclude that the observed differences in the plasticity of the digestive tract between males and females of Anas rubripes can result from different adjustment of both sexes to a temporary hunger during wintering.

The analysis of the correlations between the body size and the digestive organs parameters of the investigated group of Aythya fuligula indicated one significant relation, ie. between the total length of ceca and the length of sternum. The remaining parameters of the digestive organs did not correlate with any body measurements of the investigated birds. A number of researches indicate a lack or few significant relations between the intestine length and the body size [21,27,28]. No significant relation between the intestine length and the body size was indicated in Melanitta nigra, Anser fabalis nor Anser albifrons [4,27,28]. However, conversely to the examined Aythya fuligula, no relationship between the length of the paired ceca and the body parameters was also indicated in the three mentioned above species. The lack of correlation between the length of small intestine and the body parameters can result from the function of that organ in the processes of digestion and absorption as well as its size. This is the longest part of the avian alimentary canal and characterized by a considerable plasticity. This organ responds relatively fast with a change of its length to the diet alterations. Whereas the indicated positive significant correlation between the lengths of the paired ceca in the examined group of Aythya fuligula and the sternum can result from a different role of the ceca in relation to the remaining part of intestines during the wintering.

The analysis of the correlations between average parameters of the alimentary canal conducted for the examined group of Aythya fuligula indicated a negative significant relation between the lengths of esophagus and the small intestine and the total length of the alimentary canal. In the case of Anser fabalis no significant relationship between the lengths of esophagus and the remaining parameters of the alimentary canal was noted [28]. Similarly, the investigation conducted on Mellanitta nigra indicated no significant relationship between the lengths of esophagus and the remaining parts of the alimentary canal [4]. The positive correlation between the length of small intestine and the total length of the alimentary canal indicated in the examined group of Aythya fuligula is directly related to the size of this organ. The lack of significant correlation between the lengths of ceca and small intestine assessed in the examined group of Aythya fuligula can be related to the different role of those two organs. The well-developed ceca of Aythya fuligula are responsible for the digestive process, and due to that, they might be subject to different morphological changes in response to the diet alterations. The pace of those changes may differ from those in the small intestine which is also responsible for the absorption of food.

CONCLUSIONS

Apart from the observed sexual dimorphism in the body size of Aythya fuligula, it has not been assessed in the lengths of the analyzed parameters of the alimentary canal. Solely in the case of esophagus, it was considerably longer in drakes as compared to the females.

The small intestine was longer in the immature specimens of Aythya fuligula, both in the group of males and females, as compared to the adult ones.

A significant relation between the parameters of the alimentary canal and the avian body was only noted  in the case of the cecum. The remaining parameters of the alimentary canal did not indicate any relationship with the measurements of the body size.

The analysis of correlations between parameters of the avian digestive tract indicated a negative statistically significant relationship between the lengths of esophagus and small intestine and the total length of the alimentary canal as well as a positive relationship between the lengths of small intestine and the total alimentary canal.

REFERENCES

Accepted for print: 17.12.2008

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