Soil-Eating by Grey Parrots in Cameroon: An Answer to Mineral Deficiencies or Toxins in the Diet?
A Thesis Submitted to the Department of Agriculture; by CAROLYN SANDRA BENTLEY; In Partial Fulfillment of the Bachelor’s Degree in Biochemistry, THE UNIVERSITY OF ARIZONA; May 1999.
ACKNOWLEDGMENTS
I would like to begin by thanking Dr. Irene Pepperberg for offering the class “Do Animals Think?” my freshman year. Not only was it a wonderful practicum for the critical eye required in scientific study, but it introduced me to the interesting work conducted in her lab. Through independent study with the infamous (and stubborn) Alex, cute Grif, and crazy Kyo, I met Diana May to whom I am very grateful for providing a working hypothesis to and the chance to accompany her on her second trip to Central Africa to study these “soil-eating Greys”. And, of course, without the financial support of Irene, the UBRP program (with Carol Bender’s permission — thank you!), and the Honors Center, none of this would have been possible. A big thank you again goes to Irene and Diana for their support and for editing and revising those dreaded grant proposals.
I would like to thank the Cameroon Ministry of Scientific and Technical Research for permission to conduct this study and to Leonard Usongo, Tim Davenport, and Asonganyi of WWF-Cameroon for their logistical assistance, including transportation and plant identification. I am most grateful to Drs. James Riley, Carlos Martinez del Rio, Jamie Gilardi, and Bill Mahaney for their assistance. Funding for myself was provided by the University of Arizona Undergraduate Biology Research Program and by grants from the University of Arizona Honors Center, to Diana May from American Museum of Natural History (Frank M. Chapman Award for Ornithology), WWF-U.S. Species Action Fund and Grey Parrot Program (grant number AC52), and to Irene Pepperberg from the National Science Foundation (grant number IBN-9603803).
ABSTRACT
Geophagy, or soil-eating, is widespread among vertebrates, including humans. Proposed hypotheses for uses of soil consumption are as a digestive aid, mineral supplementation, buffer of gastrointestinal pH, detoxifying agent, and gastrointestinal cytoprotection. By studying various species that engage in geophagy, we can gain a better understanding of this behavior. May (1996) observed that Grey parrots (Psittacus erithacus) in a Congo basin forest engage in extensive ground foraging, possibly ingesting soil as well as plants. That the birds expose themselves to aerial predators during such foraging suggests that this behavior has an adaptive function. We subsequently observed Grey parrot feeding behavior in Lobéké Reserve, southeastern Cameroon. We found evidence of geophagy and plant ingestion and collected representative soil and plant samples to analyze nutrient availability and other properties. Although Gilardi (1996) found that Peruvian parrot populations most likely consume clay as a neutralizing agent for toxic seeds in their diet, the high sand versus clay content of soil collected in Cameroon suggests that parrots foraging at our study site consume soil for alternative reasons. Soil analysis supports the soil’s possible role as a digestive aid and in mineral supplementation.
lNTRODUCTION
The Grey parrot (Psittacus erithacus), widely distributed across equatorial Africa (Forshaw 1989), is common in the international pet trade (Dändliker 1992), but little is known about its nutritional needs. A recurring problem for Greys in captivity, calcium deficiency, has yet to be solved (Goodman 1996), particularly with respect to understanding how this species satisfies its dietary requirements in the wild (cf. Chapman, Chapman, and Wrangham 1991, Dändliker 1992, Forshaw 1989). Although thorough documentation of foraging behavior exists for a variety of other tropical parrots (Galetti 1993, Munn 1992), this information indicates that diet requirements and preferences vary significantly from species to species (Brue 1994). Thus, data on one species may not be relevant for another. Furthermore, few studies have addressed the relationship between food selection and plant and soil chemistry in order to determine ways that nutrient needs might be satisfied in the wild.
Recently, May (1996) observed Grey parrots foraging extensively at an exposed mineral lick in a rainforest clearing in Dzanga-Ndoki Park, Central African Republic. That the birds would expose themselves to aerial predators during such foraging suggests that this behavior has an important adaptive function. Therefore, we began preliminary tests of the hypothesis that the plants and soil are a critical dietary supplement for Grey parrots We observed Grey parrot foraging patterns in a nearby Congo basin forest, the Lobéké Reserve in southeastern Cameroon, and found that their foraging activity was concentrated in selected areas of a large swamp clearing and that feeding focused on soil and several plant species We collected soil and plant samples for analyses of nutrient availability and other biochemical and physical properties, but for the present study concentrated on soil use.
GEOPHAGY
Although still a poorly understood phenomenon, soil-eating, or geophagy, is a widespread practice among vertebrates, including our own species. Its existence challenges the common presumption that plant (and sometimes meat) consumption provides all basic dietary needs. Abrahams and Parsons (1996) recently suggested that the absence of soil in our children’s diets (eg , through ingestion of playground dirt, outdoor dust, etc.) has contributed to the declining efficiency of their immune systems. Nutritional and pharmacological explanations have been offered for human geophagy in tropical Africa (e.g., pregnant women who eat soil may be deficient in calcium and other minerals; Johns 1990).
Prevalent hypotheses for human and/or nonhuman soil consumption were summarized in Gilardi (1996) as: a) grit as a digestive aid (usually for birds, cf. Best and Gionfriddo 1991); b) mineral supplementation (Jones and Hanson 1985, Kreulen 1985, Hunter 1993), c) buffering of gastrointestinal pH (Oates 1978); d) detoxifying agent (Hladik and Gueguen 1974, Johns 1990, Johns and Duquette 199l); and e) gastrointestinal cytoprotection (Rateau et al. 1982, Kreulen 1985, Vermeer and Ferrell 1985, Mahaney et al. 1996).
EXISTING MODELS USED TO EXPLAIN GEOPHAGY
Models to explain geophagy are based on the above hypotheses. These models are non-exclusive. An understanding of geophagy is thus best obtained by eliminating one or more models rather than proving one correct.
Grit as a digestive aid model
Granivorous birds commonly consume larger particles of soil (0.6–3.4 mm), grit, which is stored in the gizzard to aid in mechanical digestion of seeds consumed (Best and Giofriddo 1991). Grit ingestion is positively correlated with the coarseness of the seeds in the birds’ diet (Best and Gionfriddo 1991). The size of the particles preferred depends on the species, but Best (1996) showed that “mean grit size increased linearly with the log10 of the body mass.” Parrots that remove the seed coat and crush the seed prior to consumption have a somewhat smaller gizzard than granivorous birds who swallow their seeds whole and, thus, must rely on the gizzard to remove the seed coat (Klasing 1998).
Support for consumption of soil — grit — as an aid in mechanical digestion includes the following: (1) preference for soil consisting of larger particles (0.6–3 .4 mm), especially grit that correlates with body mass, (2) grit found in the gizzard, and (3) a less elongated-shaped gizzard (Otani 1967, from Sturkie 1986).
Evidence that would oppose the grit hypothesis includes: (l) small soil particle size (<0.6 mm), (2) lack of grit found in the bird ‘s gizzard, (3) a more elongated-shaped gizzard (Otani 1967), (4) consumed soil granules that break down rapidly in the gizzard (e.g., bentonite clay, gypsum, and cellulose complex break down within one hour; silica, however, is persistent and thus more likely to be used as grit; see Best 1996), and (5) negative correlation between soil consumption and coarseness of diet.
Mineral supplementation model
Soil licks are probably most commonly known as ‘salt licks’ in reference to ungulates that frequent areas to obtain sodium otherwise lacking in their diets. Sodium, calcium, and magnesium are minerals found in the greatest abundance at these licks (reviewed by Jones and Hanson 1985). Sodium is the most common limiting nutrient in many animals’ diets but lack of calcium is also known to cause major physiological problems. Seasonal changes can cause fluctuations in the minerals available both in the animals’ normal diet and in the soil. When the animal’s diet is lacking in a mineral the animal may seek this mineral elsewhere. Studies have shown, however, that some parrots (Amazona, Pionus, Trichoglossus) can detect sodium levels only when the concentration is greater than 3000ppm (Cade 1964).
Support for the mineral supplementation hypothesis includes: (1) high total and available mineral content in the soil, (2) detectable sodium levels (according to the literature, detection level for Greys is unknown), (3) a given mineral concentration that is higher in the soil than in the bird’s diet, and (4) the clay mineralogy is of a 2: I structure (Davies and Baillie I 988). However, humans prefer 1:1 minerals for their lower activity which causes a “lower risk of disruption to the uptake of iron, zinc, and other micronutrients” (Davies and Baillie 1988).
Buffering agent model
Animals may eat foods that require buffering. “The rapid anaerobic fermentation of highly digestible foods in the enlarged forestomach of colobine monkeys can lead to copious production of volatile fatty acids, and the concomitant decrease in forestomach pH may cause fatal ‘acidosis’ (Goltenboth 1976). The possible antacid function of ingested soil is attributed to the buffering capacity of the clay fraction’s exchange capacity, both permanent and variable, and its ability to absorb organic molecules, including fatty acids” (quoted from Davies and Baillie 1988). The same needs may exist for birds.
Support for the buffering agent model includes: (1) the soil acts as a buffering agent in vitro much like over-the-counter antacids, (2) the soil has a high cation exchange capacity (CEC), (3) the soil can absorb organic molecules, including fatty acids, (4) the animals’ diet focuses on highly digestible seeds and/or succulent, young leaves with high protein levels. Evidence for rejection includes: (1) the soil cannot act as a buffering agent in vitro, (2) Greys show distress when fed soil with something known to alter the pH balance, (3) Greys are observed to have diverse diet, and (4) the soil has a low CEC.
Detoxifying agent model
Soil can act as a detoxifying agent when it shows strong absorption of tannins and toxins (organic molecules; Hladik and Gueguen 1974, Johns 1990, Johns and Duquette 1991, Hladik 1977, Oates 1978). Support for this model includes: (1) high tannin content in bird’s diet, (2) increased soil consumption correlating with high tannins and toxins, and (3) soil with a 2:1 clay lattice. Evidence for rejection can include: (1) geophagy and tannin concentration show a negative correlation, and (2) soil has a 1:1 clay lattice structure, which is less active due to a relatively coarse particle sizes, low specific surface, and low CEC.
Gastrointestinal cytoprotection model
Clay can line the mucosal surface of the gut for a protective effect (Rateau et al. 1982, Kreulen 1985, Vermeer and Ferrell 1985, Mahaney et al 1996). Support for this model includes: (1) a slow soil passage rate in the bird, (2) clay mineralogy is smectite or attapulgite, and (3) the soil is composed of high surface area clays. Evidence that disfavors this model includes: (1) a fast soil passage rate, and (2) soil composed of low surface area clays.
STUDY AREA AND METHODS
Study area
Lobéké Reserve occupies an ~2000 km2 area of semi-deciduous evergreen and swamp forest within the northwestern comer of the Congo basin in southeastern Cameroon (Fig. la). Two rainy seasons exist with peaks in April and October; annual precipitation is 1600–1700 mm per year (WCS 1996). The study area was Bolou savanna (~ l km2) , one of several swamp clearings in Lobéké (Fig. lb). The area includes a variety of tall grasses, various water-plants, bare soil patches, and both flowing and stagnant water areas. Along the edges of, and interspersed within, the savanna are groups of large shrubs, palms, and deciduous trees. Although the area was recently designated a reserve, pigeon trappers frequented the savanna.
Species
I studied the Grey parrot (Psittacus erithacus). I observed Grey parrots foraging in large groups (200–800 parrots) on the ground.
Diet and microhabitat
All observations were made from late June to mid-August during the long rainy season.
I concentrated sampling efforts at the study area between 0630–1100. l observed foraging directly from a blind and noted locations of vocalizations and flight directions of nearby groups. I recorded the frequency distribution of foraging Greys at these selected sites within Bolou savanna.
Methods
I noted the amount of time that at least one parrot remained on the ground, time of day, number of Greys, plant identity, and plant part consumed or “chewed”. I collected plant samples from plants bordering those that the Greys consumed and soil samples from sites where geophagy took place that day. Specifically, I scooped soil samples at the approximate depth of the parrot beak marks from patches evident of geophagy.
All soil analyses were performed by the Soil, Water, and Plant Analysis Laboratory (SWPAL) at the University of Arizona following the methods used in earlier studies of psittacedeae food selection (Gilardi 1996). SWPAL determined ‘available’ and ‘total’ mineral content of Na (total only), Mg, P, S, K, Ca, Cr, Mn, Fe, Co, Cu, Zn, Mo, and Pb using inductively coupled plasma optical emission spectroscopy (ICP). An acid digestion was done on the soil samples using nitric acid in a CEM microwave to obtain ‘total’ values; a NaCl extraction was done to simulate a parrot’s stomach to obtain ‘available’ values. CEC was analyzed using the NaCI/MgNO3 method, and particle size density (PSD) was analyzed using the hydrometer method. The same methods of analysis as Gilardi were used so that I could compare my results with his work on geophagy in neotropical parrots (Gilardi 1996).
RESULTS
PATTERNS OF ACTIVITY
Ground foraging events occurred between 0730 and 1100, typically around 0900 and averaging 40 minutes in length. Parrots leave their roosts (Dändliker 1992) before dawn to gather in perimeter trees of Bolou savanna. Single parrots, pairs, and small groups cross the clearing (or savanna) periodically. Groups steadily increase in size; vocal activity also increases. The parrots congregate in “assembly points” surrounding the site in which the entire flock will eventually forage (Ward and Zahavi 1973).
When one parrot lands on the ground to feed, others land within seconds. Next, groups from other areas of the clearing join the larger flock. The group on the ground rapidly increases in size as Greys swoop in from trees from the immediate area, landing within approximately one meter of the parrots already feeding. Although parrots on the ground rarely vocalized, parrots in the trees vocalize extensively, especially when in large groups (200–800). Small groups (<50) that are engaged in foraging activity, including both the individuals on the ground and in the surrounding trees, are often almost silent.
PATTERNS OF HABITAT USE
Parrots foraged in sites with similar characteristics. They landed in saturated to supersaturated soil bordered by grasses. Approximately 40–60% of the perimeter of this area is bordered by palms, deciduous trees, and shrubs located within 5–20 meters of the bare soil patch perimeter.
The Site Frequency graph (Fig. 3) illustrates the weekly distribution of birds at each foraging site (Fig. 2). In the first four weeks, foraging activity was dispersed over Sites I-V. The birds moved among these sites, especially Sites I, II, and Ill, daily. In contrast, during the last four weeks they concentrated their feeding at a selected site for multiple days, especially at Site VII, and including Sites VIII and IX. After a persistent rain during Week Four, Greys concentrated all ground foraging at Site VII. When the moisture had visibly dried. the parrots fed exclusively at Sites VIII and IX.
The parrots never foraged at Site Z Site Z was the only other bare soil patch I observed in Bolou savanna. It resembles Sites VIII and IX in vegetative qualities, but the distance to refuge was greater than 100 feet in all directions. Interestingly, Site Z was frequented by hundreds of green-fruited pigeons almost daily. The pigeons also foraged at sites frequented by the parrots.
PATTERNS OF FORAGING BEHAVIOR
Parrots engaged in geophagy at all identified ground foraging sites in Bolou savanna. Parrots ate flowers, leaves, stems, roots, and possibly seeds of ground plants; they also stripped tree branches and masticated its bark. They ate plants along the edges of bare soil areas, which are typically occupied by shorter, possibly younger, plants. Ground plants consumed by the Grey include: Cyperus spp., Rynchospore corymbosa, Eleocharis acutagula, Oldenlandia lanafolia, and Echinochloa cruspavonis. Greys also consumed the seeds of the tree species Celtis tessmannii, Myrianthus arboreus, and Pterocarpus soyauxii (Table 1).
May and I also observed bark chewing (in additon to ground foraging) by small groups of Greys at the savanna. On 28 and 29 June, we observed Greys chewing branches of a tree, Kigelia pinnata (a.k.a. Kigelia africana) of the Bigonciaceae family. This behavior consists of clipping off a chunk of bark, chewing the piece for several to 20 seconds (and possibly longer), and then dropping the remaining bark while clipping off a new piece of bark. Although parrots in captivity are notorious for chewing almost anything, we made two noteworthy observations: (1) Relative to neighboring trees, the trees on which Greys chewed were extensively stripped of their bark. (2) Greys clipped and chewed bark in a very meticulous manner. These observations led us to hypothesize that Greys were targeting particular trees and that they extract something from the bark while not actually consuming all or most of the bark fiber.
ADDRESSING THE MODELS
Grit model
We observed the Grey parrots remove the seed coats before consumption of the seeds of Celtis tessmannii Rendle, Pterocarpus soyauxii Taub., and Myrianthus arboreus and that sand (0.05–2 mm) dominated the soil patches’ compositions (37.1–79.4%). However, we do not know what the percentages are for soil particles within the defined range of grit, 0.6–3 4 mm. Figure 2 below shows the distributions of soil particle size for Sites I-VI and the pigeon site. Sand dominated all sites; clay content was low. By comparing Figure 2–4 with Figure 1, we can also see the changes in soil characteristics over time (weeks).
Mineral supplementation model
Sodium, calcium, and magnesium are the minerals found in greatest abundance at these licks (see Jones and Hanson 1985). Soils analyzed in this study meet the criteria for sodium detection noted above, although Site IV has sodium levels of only 2995 ppm (Fig. 3).
Buffering agent model
When highly digestible foods are ingested in great quantities, a large production of volatile fatty acids and the accompanying decrease in gastrointestinal pH may cause “acidosis” (Davis and Baillie 1988). We observed the Greys eat seeds and young leaves of the marsh pants, which are considered highly digestible foods. Additionally, the soils have an extremely high cation exchange capacity (Fig. 4). Both observations support (but do not prove) the soil’s possible role as a buffering agent.
Detoxifying agent model
Animals ingest many toxic plants, especially seeds, in their normal diet. Although we do not know the toxicity of the parrot’s diet, we can look at the soil’s role as a potential detoxifying agent. Detoxification ability is attributed to a soil’s cation exchange capacity, which absorbs toxic, or organic, molecules. The soil collected at Bolou savanna shows extremely high CEC (meq/100mg) at all sites (Fig. 4).
Cytoprotective effect model
The soil’s role in providing a cytoprotective effect to the gastrointestinal tract is attributed to the clay fraction lining the mucosal surface of the gut. Soil eaten by the Greys did not contain high clay contents (Fig. 2). Therefore, this model is an unlikely determinant of geophagy.
COMPARISON WITH NEOTROPICAL PARROTS
Gilardi (1996) observed neotropical parrots engage in geophagy at a clay lick in the Peruvian Amazon. He found high clay/low sand content and high CEC capacity in the Amazon study area in contrast to the low clay/high sand content and high CEC of our study area. Gilardi found that parrots in Peru prefer soils with a high clay content and CEC (57.4% and 28.0 meq/100g, respectively; eaten from vertical soil banks). The average soil content of the Peruvian clay was only 4.64%. With the exception of sodium, the mineral availability in the Peruvian soils did not exceed the content of minerals obtained in their diet. However, the level of sodium present was not high enough at the majority of the sites to be detectable by the birds (Jones and Hanson 1985, Cade I 964). He therefore concluded that birds do not eat soils for aid in digestion nor for mineral supplementation, but most likely as a neutralizing agent for the toxic seeds consumed (Gilardi 1996).
We found that the soil consumed by the Grey parrots in Bolou savanna shows a high content of sand (63.5%), a relatively low clay content (12.3%), and high CEC (38.3%). High CEC also can be attributed to the high organic matter present in these soils. Therefore, our data suggests that consumption of soil both as an aid in digestion and as a detoxification agent are possible reasons for the geophagy observed. Interpretation of mineral availability is in preparation.
DISCUSSION
This study brings new insight into Grey parrot foraging behavior in the wild and should contribute to a more comprehensive understanding of geophagy. Too, evolutionary implications exist for the direct comparison of an adaptive function between neotropical and Old World parrots. I describe types of foraging sites, environmental conditions that affect site use and materials eaten. I used neither scan nor focal sampling methods because (1) individuals lack distinctive plumage patterns and thus are difficult to track (for any length of time) and (2) behavior is occluded by vegetation and other individuals (because Greys forage in large, clustered groups). Data collected on plants eaten may represent only the seasonal diversity of the Grey parrot’s diet; i.e., may be true only for this area at this time.
Greys may communicate about where to feed, either through flight maneuvers or vocalizations produced when groups “congregate in assembly points” (Ward and Zahavi 1973). Future studies should focus on risk of predation based on predator approach and foraging site visibility (see Cowlishaw 1997).
Even a more complete study with more samples from non-foraged sites would still not allow definitive conclusions to be drawn about the reasons for geophagy in Grey parrots in our study site. The parrots foraged in such large groups (200–700) that they covered the entire site; therefore, the entire area was potentially a preferred site. The one non-preferred site, Site Z, that I sampled was the only bare soil patch (characteristic of all the sites that the Greys were observed foraging at) that I was able to identify as a possible alternative. Z was visited daily by large flocks of pigeons that sometimes foraged at sites that the Greys frequented. However, this site differed from the preferred sites because it was not surrounded by nearby refuge/cover vegetation.
The analyses performed by SWPAL provided some data for a direct comparison with work done by Gilardi (1996) on geophagy in neotropical parrots. Gilardi found that neotropical parrots in Peru preferred soils with a high clay content (eaten from vertical soil banks). He concluded that birds do not eat soils to aid in digestion (which would require larger particle size), but rather as a neutralizing agent for the toxic seeds consumed. Based on the texture of the soil collected in the Bolou clearing of Lobéké Reserve, I hypothesize that Grey parrots foraging at the Bolou site consume soil for different reasons than neotropical birds. The soil texture observed indicated relatively high sand/silt content as opposed to clay content, which would indicate a stronger correlation with the soil’s role as either a digestive aid and/or mineral supplementation.
Given that ground foraging behavior puts the parrots at risk for predation, we propose that such foraging behavior has an important adaptive function. We suggest the function related to nutritional needs. We witnessed avian predation on two separate occasions. And, according to our field guides, snake predation is also possible. Predation might be countered by possible sentinel behavior, large group size, selection of foraging site, as well as other adaptive behaviors, such as alarm calling. Clearly, additional study on the natural history of the Grey parrot will help put our study into perspective.
Our study, although preliminary, will have two beneficial outcomes for Grey parrots. First, our data will hopefully aid in the conservation of Greys and the forest in which they inhabit by (a) identifying which dietary requirements would be lacking if their natural habitat is destroyed and (b) determining the Grey’s role in an important tropical rainforest ecosystem. Second, results will likely assist health maintenance of captive Greys by providing at least some information on an optimal diet. Knowledge of the dietary preferences of free-ranging Greys “may suggest nutritional requirements and will help provide psychological stimulation that could enhance breeding success” (Clubb & Flammer 1994).
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