GASTROINTESTINAL MICROFLORA OF MUTTON BIRDS (PUFFINUS TENUIROSTRIS) IN RELATION TO "LIM IY" DISEASE
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GASTROINTESTINAL MICROFLORA OF MUTTON BIRDS (PUFFINUS TENUIROSTRIS) IN RELATION TO "LIM\IY" DISEASE ROSE MUSHIN AND FRANCES M. ASHBURNER School of Bacteriology, University of Melbourne, Victoria, Australia Received for publication December 21, 1961 ABSTRACT parents cease to feed the chicks, and during the MUSHIN, ROSE (University of Melbourne, starvation period the youngsters leave their burrows in search of food. At the end of April and Downloaded from http://jb.asm.org/ on March 23, 2021 by guest Victoria, Australia) AND FRANCES M. ASH- BURNER. Gastrointestinal microflora of mutton beginning of May, the mutton birds leave the birds (Puffinus tenuirostris) in relation to "limy" island to migrate to the northern Pacific. disease. J. Bacteriol. 83:1260-1267. 1962.-The In the course of the biological study of this aerobic bacterial intestinal flora of mutton birds, species, some of the chicks were found to be healthy and affected with "limy" disease, was affected by an intestinal disorder called "limy" investigated, mainly in birds from Great Dog disease by the local commercial birders. As part Island, Bass Strait, Australia. A total of 1,274 of an investigation of the etiology of the disease, specimens from gut on post-mortem and from carried out by Officers of the Wildlife Section of cloacal swabs was examined. No indication was the Commonwealth Scientific and Industrial Re- obtained of a pathogenic bacterial species con- search Organization, we were invited to study cerned in "limy" disease. A study was made of the bacterial intestinal flora of healthy and the types of organisms and their distribution in diseased birds. The results are presented in this the gut of mutton birds. The sparsity, or occa- communication. sional absence, of aerobic bacterial flora in some The term "limy" is derived from the grayish- birds, especially adults, was noticed. The "limy" yellow appearance of the intestinal contents and birds, by comparison with normal chicks, had a excreta of the diseased mutton birds. The feces richer flora more evenly distributed through the and the regurgitated food have a strong repug- alimentary canal. A higher ratio of gram-negative nant odor which can be recognized at a distance to gram-positive bacterial types was recorded in from the rookeries. Autopsy examinations showed chicks; adult birds had a lower or an even numeri- the muscles to be pale instead of the usual dark cal ratio. The comparatively frequent occurrence red color, and the fat yellowish brown instead of of Proteus species, except P. mirabilis, and of ir- the normal white. Evidence was obtained of ad- regular and intermediate coliform types was vanced pathological changes in the lower part of evident. Escherichia coli type I was not a constant the intestine and in organs such as liver and inhabitant of the gut. The gram-positive flora spleen. The cloaca was usually packed with con- consisted mostly of Staphylococcus saprophyticus, cretions which could be felt on palpation and S. lactis, and Enterococcus. The possibility that which seemed to be responsible for lesions and "limy" disease may be caused by physiological occasional perforations in the cloacal wall. On factors is discussed. opening the cloaca the concretions retained the shape of the cloaca in which they were formed. Preliminary examination indicated that the An intensive study of the ecology of the Tas- concretions were of sodium urate. (The foregoing manian mutton bird, Puffinus tenuirostris (Tem- description of "limy" disease was kindly provided minck), was carried out in Bass Strait, Australia by R. Mykytowyez.) (Serventy, 1958). This species is of commercial value to the inhabitants of the Furneaux group of MATERIALS AND METHODS islands, and its uncommon habits make it a Specimens. The material for the study was ob- source of interest to naturalists. The birds arrive tained by R. Mykytowycz. The specimens, unless at Bass Strait at the end of September, egg-laying otherwise indicated, came from various rookeries begins in the third week of November, and the on Great Dog Island of the Furneaux group of chicks are hatched in January. In April the islands in the Bass Strait, Australia. Except for a 1260
1962] GASTROINTESTINAL FLORA OF MUTTON BIRDS 1261 few samples obtained in the middle of February, sucrose, and 1 % salicin-peptone-water was ob- specimens were collected between about the mid- served. For the Bethesda-Ballerup group, growth dle of March and the last week in April, 1960. in KCN and failure to liquefy gelatin was re- The study group consisted of 42 "limy" chicks, corded, and the Vi agglutination test was per- 40 healthy and 8 experimentally starved young formed. Proteus was subdivided into species, and birds, and 33 normal adult birds. Twenty-one P. rettgeri and the Providence group were con- autopsy operations were done in the laboratory firmed by a positive tryptophan ferric chloride and all others on the island. Specimens were test (Falkow, 1957). P. rettgeri strains were taken from the proventriculus, upper and lower further grouped on the basis of rhamnose, salicin, intestine, and cloaca; 16 samples were from other and arabinose fermentation (Kauffmann, 1954). organs, usually the liver and spleen. In addition, A detailed study was made of coliform bacteria, 38 cloacal swabs were obtained from living nor- and four to six lactose-fermenting colonies from mal chicks, 82 swabs from experimentally starved deoxycholate agar were biochemically examined. Downloaded from http://jb.asm.org/ on March 23, 2021 by guest chicks, and 12 samples from regurgitated food. These strains were subdivided into types on the From other localities, mostly from Montagu basis of biochemical reactions, according to Wil- Island, New South Wales, and occasionally from son et al. (1935) with the omission of the gelatin- Phillip Island, Victoria, came a total of 44 cloacal liquefaction test. The set of five tests used was swabs, which were collected at various times from labeled IMVEC. (This formula is modified normal adult and young birds. from the one representing a quartet of tests and is Biochemical and serological tests. The routine used in the School of Bacteriology, University of procedure was to collect the material into a pre- Melbourne.) The letter "E" denotes Eijkman's servative gel according to Stuart's (1956) method, test. No distinction was made between Interme- but specimens from birds sent to the laboratory diate type I and Irregular IV, and coliforms with were examined directly. IMVEC reactions - + - - + were classified as After examining Gram-stained smears of the Intermediate type I. For the indole (I) test, a material, cultures were prepared as follows. For xylol extract was used. The methyl red (M) and gram-negative bacteria, deoxycholate agar with a Voges-Proskauer (V) tests were performed on low deoxycholate and citrate content (Leifson, cultures incubated for 4 days at 37 C (Kauff- 1935) and SS agar (Difco) were used; preliminary mann, 1954), using the spot test on a white tile enrichment was in sodium selenite, followed by for the first, and adding creatine according to subculturing to SS agar. For gram-positive bacte- O'Meara's modification for the second reaction. ria, horse-blood agar with 10% "dispersol" Eijkman's (E) test was based on lactose fermen- (Imperial Chemical Industries product), which tation at 44 C (Wilson et al., 1935), and citrate prevents swarming of Proteus, was employed. As (C) utilization was observed in Koser's liquid this study was concerned with the search for in- medium. When the IMVEC reading indicated testinal pathogenic bacteria, the cultures were an irregular or intermediate strain, the culture incubated aerobically at 37 C. A few samples were was plated on nutrient agar and a single colony cultivated anaerobically on blood agar at 37 C was retested. The IMVEC formula for the four and on nutrient agar at 25 C. The degree of most commonly occurring biochemical types was growth on primary isolation was assessed as as follows: Escherichia coli type I (+ + - + -), abundant, moderate, or sparse. Irregular I (+ + - - -), Intermediate type I Unless otherwise indicated, the bacteria were (- + - - and Intermediate type II classified according to Bergey's Manual (Breed, (+ + --+). E. coli type I strains were further Murray, and Smith, 1957). For the identification examined serologically according to Kauffmann's of gram-negative nonlactose-fermenting bacteria, (1954) technique, using two sets of diagnostic representative (average, 6) colonies from each sera. The sera for the first set were prepared with positive specimen were picked from bile salt 14 enteropathogenic E. coli strains found in media and examined for biochemical reactions in association with infantile diarrhea. These sera Kligler's lactose-glucose ferrous sulfate agar were diluted and pooled into three polyvalent (Difco), mannitol-peptone-water, urea agar, and sera as follows: in the indole test. For the differentiation of Group A: 026:B6, 055:B5, 086:B7, 0111 :B4 Paracolobactrum (paracolon) species resembling Group B: 018:B21, O119:B14, 0125:B15, Salmonella, fermentation of 5% lactose, 5% 0127 :B8, 0128 :B12
1262 MUSHIN AND ASHBURNER [voL. 83 TABLE 1. Frequency of isolation (aerobically at 37 C) of bacterial types from the gut* of mutton birds L~~~~ No. of isolations of bacterial types No. and type No. of Positive Total Ratio of speci- no. of Gram-negative types (I) Gram-positive types (II) groups of bird mens specimens solations I to II Para- Proteus colon Coli- form Staphy- Entero- Total lococcust coccus Other Total no. % 40ONormal 149 107 72 229 57 20 54 131 36 52 10 98 1.3:1 chicks 8 Starved 32 32 100 74 20 4 35 59 8 3 4 15 3.9:1 chicks 42 "Limy" 164 152 93 443 Downloaded from http://jb.asm.org/ on March 23, 2021 by guest 165 35 144 344 36 54 9 99 3.5:1 chicks 33 Normal 130 35 27 52 9 0 6 15 16 16 5 37 0.4:1 adults * Proventriculus, upper and lower intestine, and the cloaca. t According to the classification by Shaw et al. (1951), also in Tables 2, 4, and 5. Group C: 025:11L, 044:74L, 0112:B11, the Enterococcus group, and were identified by 0124:B17, 0126:B16 growth in 6.5% sodium chloride broth and on Slide agglutinations were performed with 40% bile blood agar. Gram-positive rods were living organisms on large glass slides, marked in classified as Bacillus spp. on the basis of a positive squares. As none of the strains isolated in the catalase test, spore formation, and motility. The present study reacted with these sera, there was gram-negative nonsporing rods appearing on no need for confirmatory tube agglutinations. blood agar plates, when confirmed as tolerant to The second set of sera was used to detect 20 bile salt by subculture on deoxycholate agar, somatic antigens which represent coliforms occa- were not further investigated. sionally found in association with intestinal disor- Additional tests. Gastrointestinal segments ders of animals (Orskov, personal communication). from 12 mutton birds were tested for pH value These sera were diluted and pooled into the with British Drug Houses indicator papers. following groups: As many specimens from mutton birds yielded Group W: 02, 03, 025, 086, 0117 poor growth of intestinal flora, the antibacterial Group X: 01, 04, 06, 08, 09 activity of contents from gut and samples of oil Group Y: 015, 018, 021, 078, 0115 were tested, using gram-negative intestinal Group Z: 05, 045, 051, 075, 0114 bacteria. The following strains were examined: The somatic suspensions for tube agglutination E. coli, Aerobacter aerogenes, three Proteus spp., tests at 52 C with the above sera were prepared Paracolobactrum sp., Pseudomonas aeruginosa, by steaming saline suspensions from nutrient- and Salmonella typhimurium. A bacterial lawn agar slopes at 100 C for 90 min. Suspensions for was prepared on nutrient agar with a 2-hr broth agglutination with group 08 and 09 antisera culture, and either spotting or the cup technique were heated at 120 C for 2 hr to destroy the was employed using the material previouslv thermostable antigens sometimes found in those emulsified in saline. two groups. When positive results were recorded with pooled sera, further tests were performed RESULTS with the appropriate single-factor sera. Table 1 shows the frequency of isolation of Gram-positive cocci, isolated on blood agar various types of bacteria from the gut of mutton plates, were tested for catalase production on birds which were examined in the laboratory or on nutrient-agar slopes. Staphylococcus (Micrococ- the island. The alimentary canal of normal chicks caceae) strains were coagulase-tested, and the was colonized by a variety of species, both gram- negative strains were subdivided according to the positive and gram-negative, with a slight pre- classification of Shaw, Stitt, and Cowan (1951). dominance of the first group. Both "limy" and Streptococcus strains belonged predominantly to starved chicks showed a high percentage of posi-
A\nt% 19/j;62 I (GASTROINTESTINAL FLORA OF MUTTON BIRDS 1263 TABLE 2. Frequency of isolation (aerobically at 37 C) and identification of bacterial types from the gut of mutton birds No. of isolations of bacterial types Proteus Para- Coliform Staphy- Entero- Other gram-positive colon Coiomlococcuts coccus bacteria N o. and type Tota-of of bird n.o isolations > > _ _ _ __ _ _ O O Downloaded from http://jb.asm.org/ on March 23, 2021 by guest 40ONormal 229 27 281 1 1 19 26 8 8 10 2 22 14 52 6 0 0 4 chicks 8 Starved 74 9 6 5 0 3 1 0 24 0 11 0 6 2 3 0 1 2 1 chicks 42 "Limy" 443 57 53 39 16 20 15 35 10 36 56 7 18 18 54 3 4 2 0 chicks 33 Normal 52 3 6 0 0 0 0 3 0 1 1 1 4 12 16 3 1 1 0 adults TABLE 3. Frequency of isolation (aerobically at 37 C) of bacterial types from gastrointestinal segments of mutton birds No. and type No. of gram- No. of gram- Organ No. of Positive No. of negative positive Ratio of of bird g specimens specimens isolations bacterial bacterial grouns types (I) types (II) I to I no. % 40 Normal Proventriculus 35 23 66 39 17 22 0.8:1 chicks Upper intestine 40 24 60 48 27 21 1.3:1 Lower intestine 40 28 70 59 34 25 1.4:1 Cloaca 34 32 94 83 53 30 1.8:1 8 Starved Proventriculus 8 8 100 13 12 1 12:1 chicks Upper intestine 8 8 100 12 9 3 3:1 Lower intestine 8 8 100 21 17 4 4.3:1 Cloaca 8 8 100 28 21 7 3:1 42 "Limy" Proventriculus 41 36 88 101 72 29 2.5:1 chicks Upper intestine 41 34 83 83 62 21 3:1 Lower intestine 41 41 100 121 99 22 4.5:1 Cloaca 41 41 100 138 111 27 4:1 33 Normal Proventriculus 32 4 13 6 2 4 0.5:1 adults Upper intestine 33 0 0 0 0 0 0 Lower intestine 33 11 33 19 5 14 0.4:1 Cloaca 32 20 63 27 8 19 0.4:1 tive specimens and a comparatively abundant quency of isolation of various types of bacteria flora, with a higher ratio of gram-negative types from the gut of "limy" and other mutton birds. of bacteria. Specimens from adult birds often In normal chicks, some organisms, namely P. gave no growth or the growth was sparse, with a morganii, P. mirabilis, and Bethesda were seldom predominance of gram-positive types of encountered; other types, such as P. rettgeri, P. organisms. vulgaris, E. coli type I, Staphylococcuss, and In Table 2 a comparison is shown of the fre- Enterococcus, showed a higher incidence. In
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1962] GASTROINTESTINAL FLORA OF MUTTON BIRDS 1265 starved chicks, the absence of E. coli type I and TABLE 6. Biochemical classification* of 143 Proteus the presence of coliforms Irregular I and Inter- rettgeri cultures isolated from mutton birds mediate type II was noted. In the diseased chicks, 4865 4555 4806 A 5 Proteus, showing the highest incidence, was repre- "Sugar" Group Group Group Group I II ILL IV v sented by four species, of which P. rettgeri and P. vulgaris were the most commonly encountered. Rhamnose .... - + - + The comparatively frequent presence of Bethesda Salicin ......... + - + + + strains was recorded. Coliforms were often iso- Arabinose .... _ + + lated, and amongst them E. coli type I was con- siderably less frequent than the total of Irregular No. of strains I, Intermediate type I, and Intermediate type II. isolated ...... 80 57 4 1 1 In adult birds, the absence of P. morganii, P. * According to Kauffmann (1954). Downloaded from http://jb.asm.org/ on March 23, 2021 by guest mirabilis, and paracolon bacilli was noted. In all birds, gram-positive cocci were represented mainly by Staphylococcus saprophyticus, S. lactis, birds from various localities, and from chicks and Enterococcus; gram-positive rods were with "limy" disease. seldom isolated. However, "limy" birds yielded Amongst Proteus species, P. rettgeri and P. no aerobic bacterial species which would be con- vulgaris showed the highest incidence and P. spicuous by its presence in all pathological ma- mirabilis the lowest. The total incidence of terial and its absence in normal specimens. paracolons was similar in normal and "limy" The distribution of bacterial flora in various birds. Amongst coliforms, E. coli type I strains parts of the gastrointestinal tract in "limy" and were less frequently recorded than the total of other mutton birds is presented in Table 3. The other types. The incidence of gram-positive most consistent distribution of organisms bacterial types was higher in normal and starved throughout the length of the gut was recorded in birds than in "limy" chicks. As previously "limy" and starved chicks, with a higher inci- observed, there was no indication of the presence dence of gram-negative than gram-positive types. of a specific bacterial strain in the diseased chicks. In normal chicks, the intestinal segments showed Sixteen specimens, obtained from "limy" a slightly higher ratio of gram-negative, and the birds from sources other than the gastrointestinal proventriculus of gram-positive bacterial types. tract, gave no growth, or gave organisms of the In normal adult birds, the proventriculus occa- same species as those encountered in the bird's sionally yielded growth, but the upper intestine gut. possessed no cultivable aerobes; in the proventric- P. rettgeri. The comparatively high frequency ulus, lower intestine, and cloaca the bacterial of isolation of P. rettgeri prompted a further flora from these birds was predominantly gram- study of biochemical types. Of the 165 P. rettgeri positive. strains isolated, 143 strains were examined and Table 4 sets out the incidence and identity of subdivided into five biochemical groups on the aerobic bacterial types obtained from cloacal basis of rhamnose, salicin, and arabinose swabs. The number of specimens yielding growth fermentation (Kauffman, 1954), as shown in was higher than from the gut of mutton birds Table 6. Groups I and II contained a total of (Table 1). The cloacal swabs from adult birds 137 strains, group I being predominant; the gave a poorer growth than those from chicks; three remaining groups were represented by some samples had no gram-negative organisms, only six strains. Group V, which had one strain, and none yielded Proteus. In young birds, the was not listed by Kauffman (1954). The flora of predominance of gram-negative bacterial types both "limy" and normal birds contained strains and, in adults, an even ratio of gram-negative to of groups I and II, and therefore no specific gram-positive types were noted. association with the disease was indicated. Samples of regurgitated food showed similar E. coli type I. Amongst the coliform strains, types of bacteria to those found in the gut, with a 85 E. coli type I were found (7% of the total slight predominance of gram-positive cocci. isolations). Of the 14 enteropathogenic serotypes Table 5 shows the total frequency and per- associated with infantile diarrhea, only one E. centage of isolation of bacterial types from coli 0128 B12 strain was cultivated from a chick normal and starved chicks and normal adult from Montagu Island. With the use of 20 addi-
1266 MUSHIN AND ASHBURNER [VOL. 83 TABLE 7. Determination of pH of specimens from Antibiotic tests. Gastrointestinal material the gastrointestinal tract of 12 normal mutton birds occasionally showed a weak antibacterial activity No. of Proven- Upper Lower against some gram-negative strains. Of the 15 birds tested Age triculus intestine intestine specimens tested, 1 acted slightly on E. coli type I and paracolon spp., 1 on E. coli type I 9 Adult 4.3to5.5 7.Oto7.3 7.Oto7.3 and P. mirabilis, and 1 on P. mirabilis. However, 3 Chick 2.5to5.8 7.lto7.2 7.1to7.2 this activity did not seem to be uniform and significant. One of the four oil samples tested had a pigment-promoting action on P. aeruginosa. tional diagnostic sera, E. coli 018 was isolated DISCUSSION on autopsy, eight times from specimens obtained from five adult birds in one locality and once The present investigation failed to disclose Downloaded from http://jb.asm.org/ on March 23, 2021 by guest from a chick from another locality, both on particular aerobic bacteria etiologically related Great Dog Island. Further, E. coli 08 and 09 to "limy" disease of mutton birds, Previous work serotypes were found in cloacal swabs from one eliminated viruses (Mykytowycz, Dane, and chick each on Montagu Island. Therefore, Beech, 1955) and endoparasites (Mykytowycz, typing with 34 diagnostic coliform sera indicated personal communication). the occurrence of four serotypes, the 12 isolates The type and distribution of bacterial flora representing 14% of the 85 strains examined. are of interest, but it must be emphasized that Other organisms. Some specimens showed this study was predominantly concerned with gram-positive rods and cocei in smears but did aerobic organisms. Isolations under aerobic not yield aerobic growth on bile salt media or on conditions at 37 C seemed to show that some blood agar at 37 C. From a few of these samples, samples were free of organisms capable of growth organisms morphologically resembling those in on the media provided. However, direct smears smears were cultivated either anaerobically on and cultivation of a few samples under anaerobic blood agar or aerobically on nutrient agar at 25 conditions and at 25 C usually indicated the C, but the remaining specimens were negative. presence of bacteria. Possibly, a larger inoculum Determination of pH. The results of pH testing and the use of additional enrichment and selective of material from various parts of the gut of media would show that the material was not normal mutton birds are presented in Table 7. "bacteriologically sterile." Sieburth (1959), in The proventricular material from the few chicks his study on antarctic birds, did not find them examined had an acid reaction and a wider "bacteriologically sterile," although they were range of variation than specimens from adult often devoid of typical intestinal organisms. birds. Of the 12 samples tested, only one yielded In adult mutton birds, the intestinal flora was growth at pH 5.5 (P. vulgaris, E. coli type I, and usually scanty and often absent, especially in the S. lactis). The pH of the material from the upper upper gut. In healthy chicks, the microflora was and lower intestine was nearly constant, on the absent or poor in the alimentary canal of a small slightly alkaline side, and the specimens examined group of birds examined but more abundant and were either negative or contained a mixed flora. varied in the intestine of others. In "limy" Metabolic disorders (a) High protein diet? (b) Natural starvation? I Concretions of ----Proliferation of certain flora and sodium urate >-changes in distribution in gut Mechanical I- -| "LIMY" DISEASE | I Physiological stress FIG. 1. Biological factors in relation to "limy" disease
1962] GASTROINTESTINAL FLORA OF MUTTON BIRDS 1267 birds, bacteria were found in larger numbers than No infectious agent was detected in "limy" in normal chicks from the same locality, and the disease, but the biological factors concerned organisms were more consistently distributed require further study. through the upper region of the gut. The com- paratively high incidence in mutton birds of ACKNOWLEDGMENT P. rettgeri, and the absence or comparative scarcity of P. mirabilis and E. coli type I strains, We wish to thank G. G. Blake for technical is the reverse of the distribution of these assistance. organisms in the human alimentary canal LITERATURE CITED (Mushin, 1950). The isolation of one only entero- pathogenic serotype, E. coli 0128 B12, does not BISHOP, R. F., AND E. A. ALLCOCK. 1960. Bacterial indicate the mutton bird to be a significant host flora of small intestine in acute intestinal Downloaded from http://jb.asm.org/ on March 23, 2021 by guest of these organisms. On the other hand, a few obstruction. Brit. Med. J. 1:766-770. specific coliform serotypes belonging to groups BREED, R. S., E. G. D. MURRAY, AND N. R. SMITH. 1957. Bergey's manual of determinative bac- 08, 09, and 018 were cultivated. teriology, 7th ed. The Williams & Wilkins Co., Examination of mutton birds from other Baltimore. localities may indicate more clearly the sig- FALKOW, S. 1957. A screening method for enteric nificance of the aerobic intestinal flora found in organisms using a ferric chloride test. Am. J. birds from Great Dog Island. There is a Clin. Pathol. 28:99-102. possibility of the presence of antibiotics in the KAUFFMANN, F. 1954. Enterobacteriaceae. Ejnar food of some birds, e.g., acrylic acid (Sieburth, Munksgaard, Copenhagen. 1960), although in our experiments this was LEIFSON, E. 1935. New culture media based on apparently not a significant factor. sodium desoxycholate for the isolation of A few biological factors could be considered in intestinal pathogens and for the enumeration of colon bacilli in milk and water. J. Pathol. relation to "limy" disease, and these are indicated Bacteriol. 40:581-599. in Fig. 1 as follows. (i) The normal starvation of MUSHIN, R. 1950. Bacteriological aspects of gas- mutton birds may contribute to changes in troenteritis in infants. Australian J. Exptl. bacterial flora, with the proliferation of some Biol. Med. Sci. 28:493-508. types. (ii) Further, the numerical rise and change MYKYTOWYCZ, R., D. S. DANE, AND M. BEECH. in bacterial flora and wider distribution in the 1955. Ornithosis in the petrel, Puffinus ten- gut in "limy" than in normal chicks may be an uirostris (Temminck). Australian J. Exptl. indicator of metabolic disorders which in turn Biol. Med. Sci. 33:629-636. may influence further changes predisposing to SERVENTY, D. L. 1958. Recent studies on the Tasmanian mutton-bird. Australian Museum "limy" disease. (iii) The pattern of intestinal Mag. 12:327-332. flora could be an indicator or result of a physio- SHAW, C., J. M. STITT, AND S. T. COWAN. 1951. logical stress which leads to "limy" disease. Staphylococci and their classification. J. Gen. (iv) The type of diet (e.g., high in protein) may Microbiol. 5:1010-1023. contribute to the formation of a mechanical SIEBURTH, J. M. 1959. Gastrointestinal microflora blockage, possibly in the form of sodium urate of antarctic birds. J. Bacteriol. 77:521-531. concretions. When an obstruction is established, SIEBURTH, J. M. 1960. Acrylic acid, an "antibio- it is reasonable to assume that the bacterial tic" principle in phaeocystis blooms in antarc- flora above that point would proliferate to a tic waters. Science 132:676-677. greater extent, as was demonstrated in human STUART, R. D. 1956. Transport problems in public health bacteriology. Can. J. Public Health cases (Bishop and Allcock, 1960). However, the 47:114-122. reason for the initial accumulation and blockage WILSON, G. S., R. S. TWIGG, R. C. WRIGHT, C. B. is not understood. It is difficult to assess cause HENDRY, M. P. COWELL, AND I. MAIER. 1935. and effect in intestinal disorders, that is, whether The bacteriological grading of milk. Medical the upset balance of the intestinal flora precedes Research Council (Brit.) Spec. Rep. Ser. No. or follows pathological conditions. 206.
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