MORPHOLOGY AND MORPHOMETRIC ANALYSIS OF SELECTED ELEMENTS OF DIGESTIVE TRACT IN GREAT CORMORANT PHALACROCORAX CARBO SINENSIS

Ewa Działa-Szczepańczyk, Iwona Wilczyńska
Department of Zoology and Apiculture, West Pomeranian University of Technology, Poland

ABSTRACT

The investigations comprised the digestive tract of 48 specimens of the great cormorant Phalacocroax carbo sinensis – 31 males and 17 females. The analysis featured the entire length of the digestive tract TTL and the length of the following elements of the digestive tract, namely the esophagus EL, the proventriculus and the gizzard GL, the duodenum DL, the jejunum and ileum JIL, the small intestine SIL, the terminal intestine with cloaca TCL, as well as the liver weight LW combined with the sex, the age and the body size characterized by the three parameters, ie. the body weight (BW) and the body length (BL) and the sternum length (SL). The significance of the difference between the sexes within the average values of the parameters were assessed with the t-Student test. The correlation relations between the parameters were analyzed assessing the Pearson linear correlation coefficient – r. The cormorant males, evidently bigger than the females were characterized also by a significantly longer digestive tract, longer small intestine (including its parts, ie. DL, SIL), and a heavier liver. Three parameters of the digestive tract, ie. GL, DL, and TCL, out of all considered, did not indicate a significant relation with either measurements of the avian body. The analysis of the mutual relationships between the parameters of the digestive organs indicated: (1) besides GL and TCL, all the remaining parameters correlated positively with TTL, (2) the TCL measurement correlated significantly with merely one parameter, ie. EL, (3) the GL measurement correlated significantly with two parameters, ie. LW and EL, (4) no significant relationship was observed between EL and DL, SIL, LW.

Key words: Great cormorant Phalacrocorax carbo sinensis, morphometrics, digestive tract.

INTRODUCTION

As the population of Phalacrocorax carbo sinensis on the territory of Europe has increased and affected the environment, the need of thorough knowledge of the ecology and the biology of this species arises, as well as questions referring to the diet, digestion and the digestive tract structure of this species. Similarly to other birds, the intra-specific variability observed in the great cormorant in the size of the digestive organs is mainly connected with the diet. Phalacrocorax carbo is mainly a bird of prey – it mainly eats fish and less so the crustaceans and mollusks. The subspecies sinensis is the most populous among the three subspecies of the great cormorant occurring in Poland and the only one which nests on the entire area of this country.

This work aims at the morphologic characteristics and the analysis of the morphometric traits of the selected elements of the digestive tract of Phalacrocorax carbo sinensis with regard to the sex, the age and the body size of the birds.

MATERIALS AND METHODS

The study comprised the digestive tract of 48 specimens of Phalacrocorax carbo sinensis – 31 males (16 immature and 23 adult) and 17 females (10 immature and 7 adult). The birds were acquired between September and November in 2006 and 2007 in the vicinity of Lake Drawsko (located near Czaplinek in Pomeranian Province). The shots of birds were performed by hunters on an appropriate permission issued by the minister of environment.

The cormorants were divided into sex and age groups – adult and immature (according to the development of the bursa Fabricii). The body size of birds was characterized by the three measurements: weight (BW), length (BL) and the sternum length (SL). The linear measurements – the body and sternum lengths were conducted according to the method suggested by Dzubin and Cooch [6]. Those measurements were performed exact to 0.5 cm. The body weight was assessed exact to 50 g.

The digestive tract extracted during the autopsy was unfolded and devoid of an excessive fatty tissue. It was then arranged in a straight line without undue stretch, according to the method suggested by Leopold [16]. Six measurements of length of its appropriate parts were done, ie. esophagus (EL), proventriculus and gizzard (GL), duodenum (DL), jejunum and ileum (JIL), terminal intestine with cloaca (TCL), as well as the weight of liver (LW). The border line (clearly visible) between esophagus and  proventriculus was indicated by the presence of the glands in the tissue lining inside of the proventriculus. The joined length of proventriculus and gizzard included the fragment between the border line of the transition of esophagus into proventriculus and the issue into duodenum. The duodenum length (DL) constituted the initial fragment of small intestine to the duodenum-jejunum bend. The jejunum and ileum length (JIL) was measured from the duodenum-jejunum bend to the zone of transition of small intestine into large intestine, namely the place where the ceca grow out. The small intestine length (SIL) constituted the total length of duodenum, jejunum and ileum. The large intestine length (TCL) is indicated by the fragment from the center of location of the issue of ceca into the cloaca opening. All the linear measurements of the digestive tract were conducted with the soft tape exact to 0.5 cm. The analysis of the results included also the length of small intestine (JIL) and the total length of the digestive tract (TTL). The measurement of the length of  small intestine consisted of the total length of duodenum, jejunum and ileum. On the other hand, the total length of the digestive tract consisted of the total length of five above mentioned fragments, ie. the length of esophagus, proventriculus and gizzard, duodenum, jejunum and ileum, and terminal intestine with cloaca.

The measurements of the lengths of esophagus, proventriculus and gizzard, as well as the measurement of the liver weight were performed on a lesser number of the examined birds, ie. 34 specimens (22 males and 12 females). Therefore the assessment of the average total of the digestive tract considered merely that group of birds.

The statistic analysis included the assessment to the main descriptive statistics. The significance of differences between males and females within the average  measurements was assessed by the t-Student test. The study also comprised the analysis of the relationships between the parameters characteristic for the avian body size and the measurements of  digestive tract, as well as the relationships between the parameters of digestive organs, assessing the Pearson (r) linear correlation coefficient.

RESULTS

The digestive tract of Phalacrocorax carbo sinensis commencing with the oral cavity passes into a considerably long and extremely extensible esophagus. The border line between esophagus and  proventriculus is hardly visible from the outside - one organ passes into the other without a clear-cut change of diameter. Merely through the integuments of both parts of the digestive tract one can see a transition zone indicated by a change of color, resulting from the existence of the digestive glands in the mucosa of proventriculus. The transition zone between proventriculus and gizzard is also hardly visible from the outside. Only after the cut of those two parts a border line can be seen between them  resulting from a different structure of the mucosa lining their inside (Fig. 1, 2).

The basic statistics estimated for the parameters of females and males (with the significance of differences between averages indicated) and adult and immature groups of the investigated  cormorants are shown in Tables 1 and 2. The sexual dimorphism became visible in all three parameters depicting the avian body size – the males were clearly bigger than the females. The males achieved higher average values of the parameters: duodenum length, jejunum and ileum length,  total digestive tract length and the liver weight. The remaining parameters, ie. esophagus length,  length of both stomachs, and terminal intestine length did not differ significantly between males and  females (Table 1). Adult and immature specimens both in the group of males and females little differed in the sizes of the digestive organs. The young males in the nvestigated group of cormorants were characterized by somewhat higher parameters of the digestive organs in comparison to adult specimens of that sex. Conversely, in the group of females, the majority of measurements of the digestive tract achieved somewhat higher values in adult specimens than in immature ones (Table 2). Yet, the significance of differences observed between age groups in both sexes has not been confirmed statistically.

Table 1. Differences in parameters characteristic for the size and parameters of the digestive tract between males and females of Phalacrocorax carbo sinensis (M – males, F – females, n – number of specimens, – arithmetic mean, SD – standard deviation, VC – coefficient of variation, t – t-Student statistics value, NS – statistically insignificant differences, p – the probability of mistake connected from the party of hypothesis about existence the difference between average)

Table 2. Parameters characteristic for the body size and parameters of the digestive tract in immature and adult males and females of Phalacrocorax carbo sinensis (M – males, F – females, imm – immature specimens, ad – adult specimens, n – number of specimens, – arithmetic mean, SD – standard deviation, VC – coefficient of variation). Description of symbols vide Table 1.

The correlations between the parameters of avian bodies and the measurements of the digestive organs as well as between the measurements of the digestive organs are shown in  Tables 3 and 4. No significant relationship between the parameters of the avian body and the three parameters of the digestive tract, ie. length of stomach, length of duodenum and length of terminal intestine has been assessed. The length of esophagus was in a significant relation merely with one body measurement, ie. the body length. The remaining parameters of the digestive tract entered a positive correlation dependency with the exterior parameters of the avian body (Tables 3 and 4).

The analysis of the relationships between the measurements of the digestive organs indicated a positive correlation of the total length of the digestive tract with all parameters of the digestive tract, except the length of both stomachs and the length of terminal intestine with cloaca. The coefficient of linear correlation achieved a high value for the relationship of the length of jejunum and ileum with the length of duodenum, the length of small intestine with the total length of digestive tract. The length of the terminal intestine and cloaca correlated significantly merely with the length of esophagus. The length of both stomachs remained in a significant correlation with two parameters, ie. the length of esophagus and the liver weight (Tables 3 and 4).

DISCUSSION

A specific structure of digestive tract in Phalacrocorax carbo sinensis, similarly to other avian species, is closely related to the diet and the manner and frequency of feeding. Great cormorant feeds mainly on fish [10,12,18,19,29]. However, as explicitly stated, the food preferences of this species depend on the species of fish, outnumbering in a given environment [3,14,21,28]. The research of Gwiazda [11] indicated that the diet of great cormorants feeding on Masurian Lakes was dominated by the roach (71.5% in number and 40.8% in biomass) – the dominating species in those waters. Also the research conducted in Scotland indicated that the great cormorant fed on the dominating fish in the environment - they were three species of salmonids [2].

The studied group of cormorants was characterized by a high inter-specimen variability in the analyzed parameters of digestive tract. That might have been caused by a diversified diet of birds. The quantity and kind of the food undergoes considerable diel and seasonal fluctuations conditioned by various environmental factors (eg. weather conditions), as well as the diversified energetic needs of a bird in different periods of its life – in the period of hatching, feeding chicks, migrations [8,9,25,28]. The study conducted in France on the diet of the sinensis subspecies indicated that the proportion of the eaten species of fish changed considerably in time and depended on a preferred size of fish [24]. The long, very flexible, extensible esophagus and a large stomach of the great cormorant enable the intake of a large quantity of small-sized fish, as well as a smaller quantity of large fish. In the latter case the cormorant acquires more energy what might significantly modify the size of its digestive organs. 

The observed differences in the size of digestive organs in males and females of the investigated group of cormorants can result from the differences in body sizes of birds of different sex. In birds with strongly marked sexual dimorphism in the body size, it is also marked in the absolute size of the elements of digestive tract. However, the relative values of the parameters of digestive tract (with regard to eg. body measurements) do not have to reflect the regularity: the bigger bird, the larger digestive organs. Pulliainien [23] noticed that the relative length of small intestine and ceca in the wintering Willow Grouse Lagopus lagopus is larger in females of this species than in males. Pulliainien [23] indicated that in winter the body size can significantly affect the bird demand for energy. In low temperatures of the environment, the smaller body size specimens have to feed more what in turn affects the linear parameters of the intestines in those animals. It was indicated in the case of the wintering Common Scoter Melanitta nigra that evidently larger males did not differ significantly in the length of the individual fragments of small intestine in relation to smaller females of that species [5]. The differences in the sizes of digestive organs between males and females of the studied cormorant group can also result from different preferences of both sexes for a quantity and kind of food. Such differences were observed in the case of the King Cormorant Phalacrocorax atriceps albiventer, the males and the females of which differed considerably in the proportion of eaten fish species and their weight [13]. The study on the great cormorants of the sinensis subspecies wintering in Greece also indicated conspicuous differences in the feeding preferences of both sexes. They became evident in the choice of fish species, their weight and size [17]. The study of Koffijberg & Van Eerden [15] conducted on that subspecies, on the other hand, did not indicate any significant differences between males and females in the proportion of the specific fish species in their diet. That study, however, revealed considerable differences between sexes in the choice of size of eaten fish [15].

The insignificant differences in the size of specific fragments of the digestive tract observed in the age groups of the investigated cormorants could have been related to the differences of the body size of those birds. They could have also been related to a different diet of both age groups and/or various degree of parasitic infection in the digestive tract ([1, 20]. Moreover, those differences might result from a different developmental rate of the digestive organs during the animal growth [7]. Dunn [4] indicated an unequal growth of the liver and intestine during the postnatal development in Double-crested Cormorant Phalacrocorax auritus.

The intra-specific variability in the size of digestive organs in the studied group of cormorants could have also resulted from a different food, eaten by individual specimens in an appropriate time. The investigated cormorants were acquired between September and November in the two successive years. They could have been feeding on different food qualitatively and quantitatively, what consequently could have affected the quality of parameters of their digestive organs.

The analysis of relationships between the parameters of digestive organs and the body sizes of the investigated group of cormorants indicated the lack of a significant correlation of the length of both stomachs, the length of duodenum and the length of terminal intestine with all the measurements characteristic for the body size of birds. However, the length of jejunum and ileum, as well as the length of small intestine was significantly correlated with all the cormorant body measurements. Similarly, in White-fronted Goose Anser albifrons a significant positive relationship between the body weight and the length of tarsometatarsus with the length of small intestine was indicated [26]. On the other hand, in Melanitta nigra no significant correlation between the length of small intestine and the body measurements, ie. weight and length of the body and length of sternum was indicated [5]. No significant correlation between body measurements and the length of small intestine was indicated in Anser fabalis [27]. Similarly, regarding Canachites canadensis, no significant relations between the length of small intestine and terminal intestine with the body weight of that species was noted [22]. In the case of the esophagus length one significant relationship with the body measurements was indicated, namely with the body length. Similar results were obtained in the case of Melanitta nigra in which a positive relation was indicated between the length of esophagus and the body length [5].

The analysis of the relationships between the parameters of digestive organs in the investigated cormorant group indicated the lack of correlation between the length of esophagus and the length of small intestine. Similarly, no such relationship was noted in Common Scoter Melanitta nigra [5] and in Bean Goose Anser fabalis [27]. Presumably such situation might result from a different role of those two organs in the process of gathering, digesting and absorbing of food. The small intestine – the longest part of digestive tract (70% of the total length in the investigated cormorant group), responsible for the digestion and absorption of food is a very flexible organ which adapts quickly to the changes in the diet. Conversely, the esophagus of the cormorants is mostly responsible for the tentative gathering of food.

CONCLUSIONS

1. Digestive organs of the investigated cormorant group were developed properly. No macroscopic pathological changes were noted in their structure.

2. The sexual dimorphism was visibly marked in the body size of cormorants, while in the digestive organs it became apparent in the length of individual elements of intestine, in the total length of digestive tract and the weight of liver – the males achieved higher mean values of those parameters.

3. Slight differences between immature and adult birds in the size of digestive organs were not significant statistically.

4. Three out of eight analyzed parameters of the digestive tract, ie. the length of both stomachs, the length of duodenum and the length of large intestine with cloaca were not correlated significantly with any of the three exterior measurements of the body. The esophagus length correlated positively significantly only with the body length.

5. The correlation analysis between the individual parts of digestive tract in cormorants indicated:

• positive correlation of the length of digestive tract with all parameters of the digestive tract, except for the length of both stomachs and the length of terminal intestine with cloaca;

• the length of terminal intestine with cloaca was significantly correlated merely with the length of  esophagus;

6. The measurement of the length of both stomachs significantly correlated positively with two   parameters, ie. the liver weight and the esophagus length.

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Accepted for print: 17.11.2010

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