This paper was presented at the 3rd International Conference on Avian, Herpetological and
Exotic Mammal Medicine (ICARE) held in Venice Italy on March 25th - 29th 2017.
EXPLORING THE WILD DIET TO SOLVE FUNCTIONAL DIGESTIVE DIORDERS IN ECLECTUS PARROTS
The most noteworthy aspects of our investigations, namely the physical and chemical attributes of a wild diet biased towards frugivory, a highly regimented intermittent foraging behavior, and the distinctive manner in which seeds are eaten, infer an eclectus model of digestion trending towards frugivory but founded by the principles of ancestral granivory.
In captivity, eclectus parrots are commonly fed according to granivory, which explains their high incidence of diet-induced digestive problems. Such problems are averted and remedied by adopting feeding schedules that better suit a digestion model weighted towards frugivory.
The eclectus parrot, Eclectus roratus, is a large (500-600g) colorful bird, with various subspecies inhabiting the lowland rainforests of Sumba, the Moluccas, New Guinea and its satellite islands, the Bismark Archipelago, the Solomons, and Cape York Peninsular, Australia.1 This study investigated the wild diet and feeding habits of a wild population of the Australian subspecies (E.roratus macgillivray) found in the lowland rainforests of Iron Range on Cape York Peninsular, Australia. Iron Range lowland rainforests are not as extensive as those found in New Guinea. Here they hug waterways and are fragmented into patches by open forests, melaleuca swamps and land clearing with each forest being no more than 10 kilometers wide.2 The total area of rainforest across Iron Range is approximately 500km2.
Eclectus parrots have a unique and complex social system where females and their young may be fed by a surprisingly large number (up to 7) males.3 Cooperative polyandrous breeding behavior is extremely rare in parrots, being previously reported only for Vasa parrots (Coracopsis vasa) of Madagascar.4Females retain the role of incubating eggs and protecting young, and remain unavailable for further mating until their young have fledged. The males, who outnumber females by two to one, compete aggressively for access to them.5 Females guard nest hollows in emergent rainforest trees for as long as 11 months each year.6 Throughout this period, all of their food is provided by the males who forage for fruit over large home ranges (approximately 30km2).7
Birds show a typical daily pattern of heavy morning and secondary afternoon feeding.2 Daily foraging patterns are organized in this way to minimize mortality and constrained by digestive limitations. Furthermore, the risk while foraging increases with bird mass.8 This study closely monitored the daily foraging schedule of males attending their female mate with the aim of better understanding their digestive limitations.
Eclectus parrots have been described as generalist frugivores and seed eaters.9 Data on their feeding habits is the result of circumstantial feeding records offering no clear indication of their principal food resource. 10 Abundant fruit choice attractive to birds are found across the rainforests inhabited by eclectus parrots, the majority of which have soft skins and juicy flesh.11 Previous research identified 17 fruits eaten by eclectus parrots at Iron Range.12 Although fruit pulp constitutes the greatest part of the wild diet eclectus parrots also feed on seeds, aril, leaf buds, blossoms and nectar. This study identified a further 13 fruit species as eclectus food.
Despite a clear role of fruit pulp as a nutritional reward to attract seed-dispersing birds, little is known about digestive and physiological specializations among frugivores to the nutrients in fruit diets.13 Bird-dispersed rainforest fruits typically contain either simple sugars (primarily glucose and fructose) or lipids, and fruit eating birds vary in the proportions of sugary and lipid-rich fruits in their natural diets.14 The chemistry of sugars and lipids suggests the potential for behavioral, digestive and physiological specializations to these nutrient types.15 Glucose and fructose are soluble in water and readily absorbed by active and passive mechanisms whereas lipids are hydrophobic and must be emulsified and hydrolyzed prior to absorption by passive processes.16 Individual birds modulate digestive function according to the nutrient composition of their diets, processing carbohydrate-rich foods more rapidly than lipid-rich foods17 but digestive strategies among animals specialized to diets of carbohydrates and lipids respectively are not well explored. This study explores the possible digestive specializations of eclectus parrots associated with a natural diet dominated by sugary fruit pulp.
Digestive strategies of animals are a consequence of integrated morphological and physiological traits that determine the kinds of nutritive compounds that are utilized as energy sources from foods, and the rates at which these nutrients, or their digested products, are assimilated into the body.18 Digestion of nutrients may involve competition between retention time (how long foods are retained within the gut) and thoroughness of digestion and/or absorption because retention time sets the upper limit of intake rate.19 Thus intake rate and digestive efficiency of particular dietary compounds describe the final products of a suite of physiological and morphological traits that determine the digestive strategies of animals.20
Considerable research has been directed towards understanding the morphological and physiological adaptations of digestion in frugivorous passerine birds21, and omnivorous chickens.22 Morphologic adaptations of the digestive tract to nectarivory have also been noted.23 A growing number of recent studies have described the feeding ecology and diets of wild parrots.24 Other than those belonging to the family Loriidae and obligate frugivores such as Pesquet’s Parrot Psittrichus fulgidis foraging parrots often discard fruit pulp in favor of the seeds inside.25 Most of these recent studies classify parrots as pre-dispersal seed predators, regardless of geographic region or habitat type. Seeds comprised up to 70% of the diet of free ranging parrots in the Peruvian Amazon.24 These research findings, which support the historical view that the digestive capacity of parrots has evolved around granivory, underpin current dietary strategies for most parrots species (other than those belonging to family Loriidae) kept in captivity.
From a morphologic perspective the digestive tracts of birds are built the same but vary in design depending upon the type of diet consumed. Functional adaptations are required to accommodate the physical and nutritional characteristics of the food.26 It is expected that variations in digestive morphology are present amongst parrot genera due to differences in their natural diets. 27
While alimentary tract morphology is generally regarded as distinctly tailored to the predominant diet of a species, work on passerines and poultry has shown that alimentary structures are remarkably adaptive to different diets, even with an individual.28 It has been possible to alter the thickness of the ventricular musculature and intestinal length in as little as 17 days by modifying the diet.29 Some parrots are expected to possess morphologic and metabolic plasticity, which is a hallmark of omnivores such as chickens. In this respect, Blue-and-Yellow Macaws Ara ararauna is a prime example. Unlike most congeners, which live in the Neotropical forests, it inhabits many different habitats ranging from dry savannah to tall rainforest. 30 Described as a nomadic frugivore and feeding generalist it exploits a wide variety of food resources over large areas and has recently entered urban settings in search of suitable food sources.31 Digestive flexibility is considered less robust in specialist granivores and frugivores than for those birds that eat a greater variety of food types.32 Budgerigars as specialist granivores and Eclectus as fruit pulp foragers are therefore less likely to adapt to food types that significantly deviate from their wild diet.
Modern production practices illustrate that omnivorous chickens can live the life of a granivore, eating virtually only the seeds of corn and soya.33 Contemporary nutritional strategies for parrots follow the same feeding model as the poultry industry. There are perceived failings in this feeding system, as it is more likely to be successful in parrots whose diet is not dominated by one particular food type.
The principal purpose of this paper is to present new ideas regarding dietary strategies for eclectus parrots and other parrots that appear susceptible to digestion disorders due to a lack of digestive plasticity. In order to accomplish this aim, information regarding dietary preferences and feeding habits in the wild and a theoretical model describing the likely digestive physiology capabilities of eclectus parrots are presented.
Field sites and data sources
Foraging observations focused on one eclectus family group that claimed a Kajoolaboo tree (Tetrameles nudiflora) as its nesting place. Indigenous landowners granted permission to observe the birds at this site. Although being one of the most common emergents in the area, Kajoolaboo trees are rarely used as nest trees because they are far less likely to form suitable hollows compared with milky pines (Alstonia spp.), blackbeans (Castenospermum austral), green figs (Ficus albipila) and paperbarks (Melaleuca spp.), which are the preferred nesting trees of eclectus parrots.34 Tetrameles nudiflora are buttressed deciduous trees that can grow to 40 m high with a crown spread of 10 m. The study took place during September, October and November 2015 when Kajoolaboo trees are bare of leaves. The Kajoolaboo tree was located on a narrow strip of gallery forest about 200 m wide that followed the eastern side of a small north to south flowing tidal tributary of the Claudie River (the major river in the Iron Range region). This favorable setting allowed a distant but clear view of one of these nesting trees from a sand bank on the other side of the creek, which did not disturb the birds or affect their natural behaviors. From this vantage point every activity around this nest hole, which was located in the trunk 2 m above the canopy line, and the bare tree crown about 15 m above it was clearly seen. Observations took place for 3 hours in the morning (0600-0930 hours) and afternoon (1530-1830). Most importantly it was possible to see the movements of all birds in every direction as they left and returned from the nest tree area to forage. This was an ideal location to observe their daily foraging routine. Another observation site was located at a clearing 7 km northwest of the nest along a known flight path where passing males from this group were viewed.
Unpublished data of 17 fruits collected by Sarah Legge35 at Iron Range National Park on Cape York, Australia between December 1996 and November 2003 formed the basis of this study regarding wild diet. 15 of the original fruits and a further 13 plant parts recognized as eclectus food were found and identified during this study. Observations regarding food options occurred across the two main vegetation groupings of the area; the semi-deciduous mesophyll vine forest, which is the dominant rainforest type at Iron Range found chiefly on the alluvial floodplains of the Claudie River; and evergreen notophyll vine gallery forests that fringe the river and its larger streams. 36
Foraging observations of gallery forest took place along the Claudie River from the relatively silence of a battery powered boat. This undisturbed approach allowed close access to the trees being foraged within the gallery before the birds flew off. The boat was taken ashore and the foraged tree located. Ripe fruit and uneaten fruit remains from these trees were then collected and examined in the boat to avoid the attention of crocodiles. Photographs of the tree, its leaves as well as ripe and unripe fruit were taken for identification. John Pritchard a local botanist with over 30 years experience with Iron Range plants and botanists from the Australian Tropical Herbarium (ATH) at James Cook University, Cairns identified the fruits.
The first aim of this study, which was to piece together a foraging timetable of eclectus parrots, was realized with little difficulty because our breeding group of three males and their female mate spent much of their day in or close by the nest tree. The daily routine of adult male eclectus parrots differs substantially from that of females due to a complex social system where females spend much of the year at the nest tree either standing guard over the nest hollow or rearing young in it. Males also spend most of their day at the nest tree except when they are attending to their foraging duties, which take place early each morning and later in the afternoon. These routine foraging expeditions may take them some distance and time away from the nest tree. A strict and organized feeding schedule was observed at the study nest tree. Three males attended to the food needs of the female by feeding her in the morning and afternoon.
The trio left the nest tree at the same time each morning. The three males suddenly and quietly departed the nest tree area in one of two directions heading off together as a group at dawn twilight shortly before sunrise (0620 hours). They left mostly in a northwest direction towards the dense rainforests in and around Iron Range National Park but sometimes flew southeast towards narrow gallery forests along the coastal reaches of the Claudie River. On their outward and return journey towards the National Park they were seen following an established northwest flight pathway along the southern margins of a 7 km long tapered piece of land that is cleared for the Lockhart River airfield. There were no accessible means for observing flight paths in other directions. The males covered their 7 km journey from the nest site to the flight path observation point in less than 10 minutes irrespective of wind direction. The National Park was a further 2 km beyond the observation point. Although the males left the nest tree as one group in the morning they returned separately. Two short repetitive raucous contact calls were heard in the distance as each male approached the nest tree. The female waited in the nest or remained hidden within the foliage of a canopy tree located near the nest tree whilst her males were away foraging. She responded to the arrival of each male with a single chime like call of apparent gratitude. The first returning males glided towards the nest tree alighting in the bare crown where they were clearly visible. They waited here and did not engage with the female. When the last noisy male glided in and reached above the nest tree the other two males joined him in flight and then as a group circled the nest tree before dropping to the canopy tree where the unseen female was waiting to be fed. After about 10 minutes the female returned to the nest hole and the males reappeared from the shadows of the canopy trees and moved to the bare crown of their Kajoolaboo nest tree. In the afternoon between 1530 and 1600 hours the three males left the nest tree following a similar pattern as the morning schedule. However on occasions the third male failed to return to the nest tree that night.
The collection and identification of eclectus foods was a far more difficult task because of the difficulties involved with finding and observing the birds foraging from the rainforest floor. Clearings along the edges of fragmented rainforest offered a far better vantage point as did motoring quietly along the Claudie River. As a result the presented eclectus food list is skewed towards foods that eclectus take from subcanopy plants.
17 recorded plants were previously listed as eclectus foods.35 5 were recorded as probable foods. Of these Canarium spp. and Cinnamonum olivieri were found on the forest floor below a foraging event and therefore confirmed as eclectus food. Dissalaria laxinervus was the only fruit on the reference listed not found or examined during this study. Fruits from the reference list35 and those found in this study are divided into 3 groups according to their physical characteristics. The first group contains plants that produce fruits with soft skins and fleshy pulp; the second fruits that contain seeds surrounded by aril and the third are fruits containing edible seeds. The soft skinned succulent fruits of Canarium spp., Cinnamomum olivieri (Black Sassafras), Cissus pentaclada, Cissus repens, Ficus spp., Leea indica, Mackinlaya confuse, Melodorum leichhardtii (Acid Drop), Micromelum minutum (Lime berry), Ptychosperma elegans (Solitaire Palm), Salacia chinensis (Lolly Vine), Terminalia sericocarpa (Damson Plum), Syzygium aqueum (Watery Rose-apple), Syzigium luehmannii (Lilly Pilly) and Syzygium suborbiculare (Lady Apple) are placed in the first group. Dillenia alata (Golden Guinea tree), Cupaniopsis anacardioides (Tuckeroo), Glochidion spp. (Buttonwoods), Tetracera nordtiana (Fire Vine), Claoxylon spp. (Brittlewood), Diploglottis diphyllosteia (Northern Tamarind) belong in the second group. The third group consists of plants Acacia meloanoxylon (Black wattle), Alphitonia petrei (Pink Ash), Alphitonia whitei (White Ash), Alphitonia excelsa (Red Ash), Dodonea lanceolata var. subsessifolia (Hopbush), Grewia papuana (Grewia), Lagerstomera archeriana (Native Crepe Myrtle), Macaranga tanarius (Blush Macaranga), Macaranga involcrata (Macaranga), Polyscias elegans (Celerywood), Toechima daemelianum (Cape Tamarind) that produce seeds identified as eclectus food.
Field studies met with the same logistical barriers experienced by previous research into the wild diets of tropical parrots.31 Foraging events in the dense canopy foliage are rarely observed from the rainforest floor and eclectus parrots do not enter the immediate understory to feed because plants growing there produce little if any fruit due to a lack of light penetration from above. However, raucous calls of male eclectus gave direction to foraging sites. Our observations confirmed previous research findings that eclectus parrots spend most of their morning and afternoon foraging time within the protection of the rainforest canopy where an abundant supply of soft skinned fleshy fruits are found. 37 In our study eclectus parrots were seen eating succulent pulp from the fruit of Salacia chinensis and Leea indica. The textural qualities, water and nutrient content of these fruits are typical of canopy foods eaten by eclectus parrots, which make up the bulk of their natural diet.
Eclectus parrots are more visible away from the protection of the canopy. They are seen most often at the edges of rainforest where plants receive the necessary sunlight to promote flowering and fruit set. The best viewing is located along roadway cuttings, creeks, woodland/ grassland margins and areas disturbed by fallen trees where feeding activity occurs at a lower level than the rainforest canopy. These auxiliary foraging forays, which are usually noticed late morning, appear to focus on seeds and other foods of high nutritional worth. Hopwood Dodonea lancelata is a perfect example of nutritionally valuable eclectus food. There is substantial foraging time, risk from predation and energy cost involved in finding and eating the tiny seeds of this and similar plants, which suggest they offer a high nutrient incentive. Therefore it is expected that seeds constitute a much smaller part of the wild diet compared to fruit pulp, which further corroborates the eclectus position in the guild of frugivory.
The hard small nutritionally concentrated seeds of Dodonea lancelata and wet nutrient-dilute fruit pulp of Salacia chinensis and Leea indica epitomize the physical and chemical extremes of the eclectus wild diet. Discrepancies between the physical and chemical characteristics of these known natural foods are used to claim the distinct digestion capabilities of eclectus parrots. Close observations of captive birds consuming Dodonea lancelata seeds were responsible for unveiling an eating habit distinctly different from chicken or parrot granivory and more closely aligned with the digestive principles of frugivory. The ancestral digestion model of granivory, which has been conclusively described for poultry24, is the basis of our digestion hypothesis for eclectus parrots with elements of frugivory overlaying it.
Natural foraging behaviors and eating habits, which are considered an adaptive response to the wild diet23, were also studied because of their close association with digestive processes. Fortuitously visits to Iron Range coincided with breeding activity and a time of year when Kajoolaboo trees are bare of leaves. This annual event presented a rare opportunity to enjoy an unobstructed view of the daily movements of a family of eclectus parrots. As a result this study was able to clearly demonstrate a highly regulated intermittent feeding pattern of eclectus parrots in the wild.
The most noteworthy aspects of our investigations, namely the physical and chemical attributes of the wild diet biased towards frugivory, a highly regimented intermittent foraging behavior, and the distinctive manner in which seeds are eaten, infer an eclectus model of digestion trending towards frugivory but born upon the principles of granivory.
In captivity, eclectus parrots are commonly fed according to granivory, which explains their high incidence of diet-induced digestive problems. Such problems are averted and remedied by adopting feeding schedules that better suit a digestion model weighted towards frugivory.
The unusual features of eclectus digestion are illustrated by comparing the foraging behaviors, eating habits and characteristics of the wild diet of the Australian eclectus parrot (E.r.mcgillivrayi) with those of the sulfur-crested cockatoo (Cacatua galerita), a granivorous parrot of similar size that occupies woodlands adjacent to the rainforests of Iron Range.
Natural foraging behavior
Our observations demonstrated that eclectus parrots follow a highly regulated intermittent feeding pattern. This natural foraging behavior is aimed at increasing food storage capacity and processing large meals as quickly as possible. Our digestion model adopts the view that food holding capacity and digestion rates are maximized by this feeding pattern because meals are taken on an empty stomach.
The principles of economic design restrict the maximum food holding capacity of the upper digestive tract (crop, proventriculus and gizzard) to a weight that allows flight.29 The high moisture content of a fruit diet means eclectus parrots must consume greater food volume than sulfur-crested cockatoos or other equal-sized granivorous parrots to meet their energy and nutrient requirements. Eclectus have overcome the space limitations presented by their wet bulky nutrient dilute wild diet through evolutionary modifications to the alimentary tract. A wide flexible thoracic esophagus is a morphological adaptation that facilitates a high rate of digestion by facilitating a fast passage of bulky wet foods from mouth to proventriculus when meals are taken on an empty stomach. The proventriculus of eclectus parrots is an elongated tubular and highly distensible structure capable of holding as much food as the crop. The proventriculus of sulfur-crested cockatoos has half this capacity holding the same amount of food as the gizzard. The gizzard of eclectus parrots is an equivalent size but less muscular and more spacious and therefore is likely to hold a greater volume of food than that of sulfur crested cockatoos.30 These evolutionary anatomic alterations are directed towards an increased need to consume, store and process large volumes of wet nutrient dilute food as quickly and completely as possible.
The interpretation that gastrointestinal (GI) tract structure and biochemistry are “adaptive” rests on the assumption that the GI tract digestive characteristics regarding morphology are matched to the prevailing diet composition and feeding rate, and that these characteristics do not provide a digestive capacity in great excess of what is necessary for the prevailing diet and feeding rate.39 Polyandrous behavior suggests eclectus parrots have reached the limits of their food holding capacity in everyday life and that healthy digestive function is dependent upon their crop and proventriculus being filled to capacity at each mealtime. These inferences support the notion that taking a full meal each morning and afternoon at a precise time has a beneficial impact of increasing the rate of digestion by stimulating the cephalic and gastric phases of gastric digestive juice secretion.34
Eclectus parrots show notable differences in the way they eat food compared to sulfur crested cockatoos and other granivorous parrots. Eclectus parrots being strictly arboreal do not eat grass seeds as part of their wild diet. Even so they retain an adept ability in captivity to remove the husk of cereal grains and aster family oilseed grains before eating the kernel, a feature synonymous with psittacine granivory. Eclectus parrots masticate the de-husked kernels of these grass seeds and cultivated grains into very small pieces before swallowing it whereas granivorous parrots swallow them whole. The tiny hard black seeds of Dodonea lanceolata eagerly sought by captive eclectus parrots are also broken into small fragments before being consumed. This peculiar eating behavior, which implies a digestion adaptation aimed at easing gizzard effort and reducing the time this type of hard food stays there also suggests hard foods constitute a small part of the wild diet.
Physical attributes of the wild diet
The speed at which food passes through the proventriculus and gizzard unveils the different digestive strategies employed by frugivory and granivory. The wild diet of eclectus parrots being dominated by soft wet sugary fruit pulp requires more time in the proventriculus being processed by acid degradation and less effort and time being physically degraded in the gizzard and chemically digested in the intestines. The digestion process for granivory follows a contrary pattern39 where the digestive role of the proventriculus is strongly subordinated by the grinding actions of the gizzard and digestion activity in the duodenum.
Chemical composition of the wild diet
In birds a high diversity of gut biochemical capabilities seems to support the existence of a correlation between morphology and physiology of the intestinal tract and chemical features of the wild diet.40 Eclectus parrots appear to follow the lead of frugivory and utilize carbohydrates mostly in the form of simple sugars and digestible starch to a lesser degree as their primary energy resource.
Protein is recognized as a limited and coveted nutritional resource of frugivory.31 Nutritional analysis of the seeds of Dodonea lancelata, Alphitonia excelsa and Cupaniopsis anacardioisis suggest the wild diet of eclectus parrots is deficient in protein and fat.30 It is possible that any dietary fat shortcomings of eclectus parrots are overcome by endogenous triglycerides produced in the liver directly from hexose sugars (fructose and glucose), which are abundantly present in rainforest fruit pulp. The intermittent engorging feeding habit of eclectus parrots that initiates gastric secretion of pepsin may improve assimilation and assist protein shortfall.
Fat digestion in the duodenum is a lengthy process compared to the rapid assimilation of hexose sugars found abundantly in the fruit pulp and digestion of starch found in seeds. Fat is an unlikely energy alternative to starch for eclectus parrots that clinically show digestion bottlenecks in the proventriculus when fed nuts.30 Sulfur-crested cockatoos and macaws show no such sensitivity to nuts. The wild diet of scarlet macaws being lipid and protein rich31 indicates an adaptive digestive strategy has been evolutionarily employed for processing high levels dietary fat. Sulfur crested cockatoos are also able to efficiently digest fat, a process that eclectus parrots seem to lack because tropical frugivory tends towards carbohydrate rich, protein and lipid poor wild diets.41 Accordingly fat is a likely small part of the eclectus wild diet.
Proposed digestion model
This hypothetical digestion model for eclectus parrots adopts the principles of frugivory whilst acknowledging reliance upon ancestral granivory-based chicken digestion theories.22 Accordingly, fruit pulp rather than seeds have most influence over the digestive functions of eclectus parrots. Frugivory and granivory share the same digestion aims of processing food completely and as quickly as possible into a form that allows essential nutrients to be fully assimilated and readily available for bodily functions. A fundamental distinction between frugivory and granivory is the speed at which food moves through the proventriculus and gizzard. Fruit pulp being soft and wet spends most time in the proventriculus and less time in the gizzard being processed whereas the reverse applies to parrots subsisting on seeds, which are relatively hard and dry foods.
Gastric secretion of hydrochloric acid is key to solving functional digestive disorders in eclectus parrots as it has most control over the rate of passage of food through the proventriculus and initiates the first part of protein digestion by activating the gastric enzyme pepsin. Three phases of gastric secretion have been described for birds: cephalic, gastric and intestinal phases.43 Their combined purpose is to accelerate the rate of digestion to optimum levels by acidifying stomach contents. Functional deficiencies caused by failure of the first cephalic and second gastric phases of gastric secretion have most impact on eclectus health.
In the wild, eclectus and other large parrots like sulfur-crested cockatoos follow a strict and highly predictable morning and afternoon feeding routine. The implicit expectation of eating at the same time each day created by this natural foraging behavior stimulates the cephalic phase of gastric secretion, which is under vagal control. In birds, vagal stimulation causes more pepsin than hydrochloric acid to accumulate in the stomach.43 Therefore, the cephalic phase, which prepares for protein digestion before food is eaten, is crucial for eclectus parrots whose wild diet is deprived of protein. For captive parrots, the cephalic stage of digestion is best stimulated by providing morning and afternoon meals at the same time each day, and allowing the bird to watch or hear the meals being prepared. Chewing action, which is a distinct eating characteristic of eclectus parrots, is believed to stimulate the cephalic stage of gastric secretion. Grapes or pieces of apple that promote mastication may aid eclectus digestive function by stimulating the cephalic phase of gastric secretion.
The second phase of stomach juice production, which is under the control of gastrin, is also influenced by natural foraging behaviors. Gastrin is the central hormone involved with digestion as it controls the amount of hydrochloric acid being produced by the stomach glands. The release of gastrin is mediated by neuroreceptors located in the wall of the proventriculus and activated when food stretches the stomach wall. The intermittent natural feeding behavior of eclectus and other large parrots dictates their morning and afternoon meals are taken on an empty stomach. This means the bulky fruit pulp eaten by eclectus parrots enters, fills and stretches the proventriculus quickly to simultaneously stimulate the production of gastrin. This second phase of gastric secretion is possibly extended by the bulking actions of starch gelatinization and hydrophilic fibers found in rainforest fruit pulp, which maintain a growing pressure on the wall of the highly elastic eclectus proventriculus. For captive Eclectus, this critical second phase of digestion is supported by feeding wet, bulky meals containing a beneficial complement of hydrophilic fiber at a set time each morning and afternoon.
The third intestinal phase of gastric secretion mediated by several hormones including cholecystokinin (CCK), secretin and avian pancreatic polypeptide (AAP) seamlessly coordinates the digestion process by stimulating the full release of gastric juices (hydrochloric acid and pepsin) at precisely the same time as the second stored part of the meal leaves the crop and enters the proventriculus.
The proventriculus is regarded as the dominant organ of the eclectus digestion model as food spends most time being processed there. Although food passes much more quickly through the eclectus gizzard than that of seed eating parrots, the gizzard’s definitive role as digestion pacemaker must not be overlooked. Food particles are moved into the small intestine after they have been ground to a critical size in the gizzard. Nutrients are then digested and absorbed along the small intestine. Less is known about optimal functioning of the small intestine but stimulation of typical gizzard development will likely improve the functionality of the small intestine through better feed-flow regulation.
The size of bird intestines has been adapted to flight and is therefore comparatively short. Birds reflux digesta between various locations of the alimentary tract to compensate for this reduction in digestive capacity.44 According to this theory a reflux in parrots may also occur between the gizzard and duodenum. Hypothetically digesta, digestive enzymes, and bile are shuttled between the gizzard and duodenum to optimize the action of enzymatic and mechanical digestion in this and lower parts of the digestive tract. The speed of eclectus digestion is likely to be influenced by such a gastro-duodenal reflux through its involvement with the intestinal phase of gastric secretion. In poultry this final phase of acid production in the stomach is largely controlled by cholecystokinin (CCK), secretin and avian pancreatic polypeptide (AAP).22 Under this model AAP is released from the pancreas when amino acids and hydrochloric acid within the ingesta leaving the gizzard reach the caudal pole of the duodenum. Significantly the effect of AAP, which increases gastric acid and pepsin secretion, is independent of the vagus nerve, serves to stimulate digestion immediately the food bolus enters the proventriculus from the crop. CCK produced in the duodenum and jejunum boosts the rate of digestion by further stimulating acid secretion in the stomach whilst having no effect on pepsin secretion. Secretin stimulates both acid and pepsin secretion, which is particularly relevant for the dietary protein scarcity of frugivory. The combined effect of these hormones is to maintain a rapid rate of digestion by stimulating the full release of gastric juices (hydrochloric acid and pepsin) at precisely the same time food enters the stomach from the crop. Excessive amounts of hard fibrous foods that hinder normal gizzard function in eclectus parrots also disturb the gastroduodenal reflux process, which not only reduces the digestion of fats in the duodenum but also slows the digestion process in the proventriculus and gizzard because the hormones associated with the intestinal phase of gastric secretion have not been properly stimulated.
The prime purpose of all phases of gastric secretion is to optimize the rate of digestion by acidifying the proventriculus contents. Their full function is of greater relevance for frugivory than granivory because large volumes of fruit pulp spends more time being processed in the proventriculus.
Understanding the differences between the digestion process of granivory and frugivory helps solve digestion problems in parrots of both persuasions. Digestion function of sulfur-crested cockatoos, as an example of granivory, is defined by hard dry non-fermentable seeds, strong gizzard activity and limited time in the proventriculus. The digestive signature of frugivory and eclectus parrots is large volumes of soft, wet, fermentable fruit pulp, extended time in the proventriculus and subdued gizzard activity.
Dietary induced functional digestive disorders of eclectus parrots can be explained by gastric secretion failure whereas for granivory impaired gizzard activity is their likely cause. Solving the digestive dysfunction in eclectus parrots requires identifying the affected phase(s) of gastric secretion and dietary error associated with the failure. Acting in league with natural foraging behavior the three key physical features of the wild diet, namely bulk, moisture content and fiber balance, stimulate the full evolutionary potential of the distinctive digestive tract of eclectus parrots.
Remedial feeding strategies that chose foods with equivalent textural qualities as rainforest fruit pulp and adopts the same natural foraging behaviors as wild Eclectus can be used to reclaim healthy digestion in captive birds irrespective of the origins, complexities or persistence of their gastrointestinal complaint. Initial treatment for birds with digestion dysfunction focuses on relieving the symptoms of discomfort, which are caused by bacterial fermentation, opportunistic and/or other infections of the gastrointestinal tract related to food contamination or foreign ingested matter. With a return of appetite remedy foods are then introduced to gradually reestablish a healthy rate of digestion. Before this goal can be achieved the inciting cause of digestion dysfunction and its harmful affect on other digestion organs must first be illuminated and managed by clinical and diagnostic investigation.
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Stomach Dysfunction in Eclectus Parrot - ICARE Conference April 2019
Audio visual presentations from 2018 Atlanta AAV Conference