Mass mortality among European Common in South Africa in April-May 1961 By M. K. Rowan Percy FitzPatrick Institute of African THE COMMON {Sterna Mr undo) is a migrant to South Africa, occurring on the coasts from October to February, although some may remain throughout the year (McLachlan and Liversidge

continued...

103 BRITISH BIRDS

FIG. I . The Cape, South Africa, with arrows to the areas where many Common Terns (Sfernabiruado) died in spring 1961. This map covers a width of some 600 miles 1957). In 1961, an unknown but apparently substantial proportion of the migrant population lingered long after the usual departure date and during April many became ill and died. High mortalities were observed at several localities from Port Elizabeth in the east to Lam­ bert's Bay in the west (see Fig. 1) and the affliction may have been even more widespread. In the investigation of this event, help was received from many quarters. For assistance in the laboratory and the field, I am indebted to Dr. G. J. Broekhuysen, J. G. R. MacLeod, J. Martin and Dr. J. M. Winterbottom. Otner observations of dead and healthy birds were kindly made available by Mrs. M. Atkinson, Mrs. S. Barnard, A. R. Brown, M. Chaundy, Miss Krynauw, K. Krynauw, O. Lawson, Captain G. M. le Gras, R. Liversidge, Dr. Elsabie Malan, Miss L. Olivier, J. Rossow, Mrs. L. D. St Leger Searle and J. Spannenberg. Finally, in the search for the cause of the disaster fullest collaboration was accorded by Professor A. Kipps and Dr. W. Becker of the Virus Research Unit, University of Cape Town, and by Dr. J. K. Thompson and Dr. P. M. S. Masters of the Division of Veterinary Services.

FIELD OBSERVATIONS Several of the field reports now available for tracing the onset and course of the mortality among the Common Terns were not submitted until some days or weeks after the observations were made. In consequence, the numbers of sick and dying birds and the dates on which they were seen were not always exactly known. It seems probable, however, that the first deaths in the south-western part of the Cape occurred during the second and third weeks of April. Some rather vague reports for this period are supported by two definite records of three dead terns at Fish Hoek in False Bay and two at Hout Bay on the Atlantic coast of the Cape Peninsula during the week

104 MORTALITY IN SOUTH AFRICA i5th-2ist April. However, it was not until the weekend of 22nd- 23 rd April that information from the Strand in False Bay brought indication of the extent of the mortality and more critical investigations were set in hand. With the assistance of MacLeod and Martin, some four miles of the shore between the Strand and the mouth of the Eerste River were systematically quartered on three separate days—23rd, 25th and 26th April. The population of living terns along this stretch of beach was then estimated at 1,200-1,500, but numbers dwindled steadily during the ensuing weeks, either by exodus or death, until on 13 th May there were less than fifty left. Apart from an occasional Sandwich Tern (S. sandvicensis), the birds were all Common Terns or Arctic Terns (S. macrurd) and no Arctic were found amongst the dead. On 26th April about half the living birds were in groups of ten to thirty at intervals along the water's edge. The rest were congregated at a shallow, slightly saline lagoon at the Eerste River mouth, which is a regular roosting site. About one-tenth of the living birds appeared to be ill. They were reluctant to fly when their companions took wing at our approach and they remained on the sand until we were within ten or twenty yards, then rose with evident difficulty and flew only a short distance at a time. Others were too sick to fly at all and were easily caught by hand. Several of the birds in this state had become separated from the flocks and were squatting singly on the dry sides of small dunes far from the water's edge. Most, however, were found at the river mouth, where the number of distressed and severely weakened terns was pathetic to see. The afflicted birds produced a copious fluid excrement. Dead birds lay scattered over the whole four-mile stretch of beach between the dunes and high water mark. Approximately 150 corpses were buried or collected (for post-mortem examination) during the first three days' work; and, at intervals during the ensuing two weeks, Martin and MacLeod buried a further 320-odd. The total (469) thus amounted to 25-30% of the estimated living population at the outset of this work, but probably did not represent a full tally since the dead birds were not easily detected in the drifting sand and a number must have been overlooked. In addition, Black-backed Gulls (Larus dominicanis) and Cape Ravens (Corvus albk'ollis) were seen feeding upon the dead, while rodents, whose burrows were abundant amongst the dunes, probably shared the macabre feast. It was, how­ ever, my impression that scavengers were fewer and less active than might have been expected in the presence of so much food. Another part of the False Bay coast where terns commonly con­ gregate is the Zeekoevlei outlet near Strandfontein. From this locality, as from the Strand, "large numbers" of dead birds were 105 TABLE I—EUROPEAN-RINGED COMMON TERNS {Sterna hirtmdo) RECOVERED IN SOUTH AFRICA IN APRIL-MAY 1961 Two relevant recoveries later in the year have also been included. With the possible exception of the three for which no data are yet available, all had been ringed as young variously classed as "pullus", "nestling" or "juvenile"; the first Finnish was described as "migrant young". The birds entered as "ist-winter" all had the dark carpal bar on the wing (page 108)

Country Date Date Place Approx. age of origin Ring no. Place ringed ringed found found Finder type at death

Sweden YM2128 59°i3'N, ij°}i'E 27.6.57 23.4.61 Strand J. Rossow "ist-winter" 46 months J. Spannenberg K. Krynauw Sweden YS1724 59°28'N, 29°i5'E 17.6.59 0.5.61 Strand E, Crewe — 24 months Sweden 537102 58°i3'N, I4°40'E 19.6.60 7.5.61 Strandfontein A. R. Brown — 10 months Finland A120565 6i°32'N, 2i°35'E 21.8.60 1.5.61 Strandfontein Dr. P. M. S. Masters "ist-winter" 8 months Finland A119807 6o°i2'N, 25°24'E 18.6.60 4.5.61 Strand Mrs. S. Barnard " 1 st-winter" 10 months Finland A130021 63°05'N, 27°35'E 6.7.60 4.5.61 Saldanha Bay G. J. Broekhuysen "ist-winter" 10 months Finland A102292 6o°i5'N, 2i°5o'E 27.6.59 4.5.61 Strand J. G. R. MacLeod — 23 months Holland ? (Makkunerwaard) 25.6,60 14.5.61 Gordon's Bay Mrs. M. Atkinson — 10 months Heligoland* 7171708 — — — 0.4.61 Lambert's Bay Mr. Groenewald — — Heligoland 7370958 53°39'N, I2°I7'E 21.6.60 4.5.61 Gordon's Bay O. Lawson _ 10 months Heligoland 7323823 53°57'N, 8°26'E 17-7-59 9.5.61 Gordon's Bay Mrs. A. Gentis — 22 months Heligoland 7284749 53°39'N, i2°i7'E 6.6.60 22.4.61 Strand J. G. R. MacLeod "ist-winter" 10 months Russiaf 213156 _ _ — 0.5.61 Strand J. G. R. MacLeod — — Russiaf F751400 _ _ _ 0.5.61 Strand J. G. R. MacLeod — — Finland A124401 6o°o6'N, 25°04'E 28.6.60 15.6.61 Strand — _ 12 months Finland A72792 6o°zi'N, 27°28'E 7-7-57 0.9.61 Walvis Bay J. J. Rossouw — 50 months

•Ringer has not yet submitted details to ringing station fNo reply yet received from ringing station COMMON TERN MORTALITY IN SOUTH AFRICA reported from 24th April onwards; and workmen engaged on canalis­ ing the vlei outlet thought that they had noticed the first casualties about the middle of the month. On 30th April Brown counted 80 corpses in one place at Strandfontein and 139 at a second. Many- others were scattered in between and he estimated the total at 270 to 300 over a two-mile stretch of beach. In a smaller area, less than half a mile long, Winterbottom, Masters and I found approximately 120 sick and dead birds on 1st May; and on 7th May Brown found a Further 5 3 newly perished in the same locality. By 12th May, however, this part of the coastline was deserted, and no terns, alive or dead, were seen. During the same period (24th April to 1st May) other casual reports were received of dead terns near George on the south coast, and at Sea Point on the peninsula. On 29th April Broekhuysen found five dead Common Terns at Langebaan, and one dead Common Tern and two dead Swift Terns (J", bergii) in a nesting colony of the latter at Meeuw Island in Saldanha Bay. In a neighbouring area, Velddrift on the Berg River, Chaundy found no evidence of any mortality on 13 th May, but noted about 50 Common/Arctic Terns in apparent good health on the river estuary and shore. Further north, at Lambert's Bay, Winterbottom and I made observa­ tions and enquiries during a visit on 23 rd and 24th May. At that time, no signs of illness could be detected amongst an estimated 200-300 Common/Arctic Terns which were frequenting the shore; but the Harbour Master, who also acts as superintendent of the neighbouring guano island, reported that "at least 400" terns had died during the second half of April, chiefly on the island where they roost and to a lesser extent on mainland beaches. In the Port Elizabeth area, Liversidge recorded mortality among Common Terns towards the end of April and during early May. He has kindly made available an interesting report from Captain le Gras, skipper of a fishing vessel, who noted dead terns in various fishing areas (5-10 miles off Cape St. Francis, off Slang Bay, and off Bird Island at about 34°S, 26°E) between 26th April and 10th May. Altogether about 40 corpses were observed floating on the water over a total area of 20-25 square miles. Le Gras added that "it is unusual to see any dead birds at sea, and the odd one found is a rare event". He also recorded a sick Common Tern which alighted on deck, refused to fly or eat, and died two days later "passing a green liquid from the vent".

RINGING RECOVERIES This disaster resulted in 14 ringing recoveries as shown in Table 1, which also lists two further recoveries made later in the year. In the past, Common Terns bearing Finnish, Danish and German rings have 107 BRITISH BIRDS been found on South African shores (McLachlan and Liversidge 1957, Anon i960, Nordstrom 1961), and the present records again suggest that the Baltic region and European North Sea coast supply the bulk of this migrant population. However, the two Russian returns, which have not yet been acknowledged by the ringing station, could refer to birds breeding anywhere in that country, more especially as a Common Tern ringed as a nestling in the Black Sea area in 195 5 was recovered a year later at East London (Anon 1956). It is interesting that British- ringed Common Terns, which breed in the same latitudes as the Dutch and German birds, have never been found in South Africa, although the total of over 31,000 ringed in the United Kingdom up to the end of i960 has resulted in 609 returns (1.95%), mainly from southern Europe and West Africa (Spencer 1961). Writing of S. hirundo in the Americas, Austin (1942) stated that "of all the recoveries made on the wintering grounds eighty per cent at least are birds of the year". Most of the earlier recoveries of this species in South Africa and eight out of the thirteen returns for which data are available were also yearling birds. However, three were in their second year, one was in its fourth, and the last was in its fifth.

LABORATORY INVESTIGATIONS Many of the dead birds seen in the field were damaged, severely dehydrated or decomposed, but about 130 specimens in fair to good condition were obtained between 23 rd April and 1st May. Several of the freshest birds, including some which were found in extremis and destroyed, were reserved for bacteriological and virological tests, while the remainder (111) were examined in the laboratory at the Percy FitzPatrick Institute with the results recorded below.

(a) Plumage Various authorities (Murphy 1936, Witherby et al. 1941, Peterson 1947) have indicated that dark lesser coverts, forming a distinct bar on the carpal joint of the wing, serve to distinguish Common Terns in their first winter from birds of greater age, although occasional individuals may retain some deep grey coverts well into adulthood (Cullen 1957). Seventy-eight of the 111 specimens in this series had the carpal bar. Most of these were probably yearlings and three ringed individuals certainly were. However, a fourth ringed bird with the dark shoulder mark had been marked in the nest in Sweden nearly four years before. The extent of the carpal bar was variable: about one-half of the specimens retained most or all of their dark coverts, but the rest were in various stages of replacing these with the paler grey typical of adult summer plumage.

108 COMMON TERN MORTALITY IN SOUTH AFRICA Most of the "first-winter" birds (those having the carpal bar) had white foreheads, but in four the feathers of this area were largely black. Among the 33 "adults" (those lacking the carpal bar), there were 15 with wholly black foreheads, eight with white foreheads and nine at an intermediate stage. The remaining two specimens were slightly damaged about the head so that the colour of the feathers could not be certainly determined. Forty-five of the 78 specimens with dark carpal bar were completely white below, but the remainder of this group and all the "adults" had grey feathering from throat to vent, the tone varying individually from a pale wash to a much deeper shade with a warm mauve tinge. In nearly all specimens (whether with or without shoulder patch), the first or second pairs of outer retrices, or both, were either missing or in process of development. The only exceptions were five birds in adult dress in which the tail moult was recently complete. Most interesting was the state of the flight feathers. Of the 78 specimens with carpal bar, the primaries had been completely and recently renewed in ten (including the four-year-old bird mentioned above), more than half of the primaries had been replaced in 5 2, and less than half in 16; secondaries had been fully replaced in 61 and were in process of renewal in 17, all except one of these being birds in an early stage of primary moult. By contrast, in all 33 "adults" the wing moult was complete, but the feathers were fresh, showing no more signs of wear than did the new primaries and secondaries of birds in the "yearling" group. This was surprising, since, according to Witherby et al. (1941), the adults of British-breeding Common Terns replace their flight feathers in a post-nuptial moult which begins in July-August, but do not appear to moult their primaries or secon­ daries twice in one year. The "first-winter" birds, on the other hand, conformed to the statement by Witherby et al. that yearlings undergo their first complete moult in the February-June following their birth. Two possibilities thus exist: (i) that the entire series of specimens consisted of first-year birds, with the exception of the five ringed ones of known greater age; or (ii) that the moulting pattern in the popula­ tions reaching South Africa differs slightly from that in British birds.

(b) Soft parts The colouring of the soft parts was recorded only for those specimens which had not suffered any noticeable dessication. Fifty birds with the dark carpal bar had wholly black bills, nine showed some red at the base of the lower mandible, and two had bills which were wholly red except at the tip. Five of those in adult dress had wholly black bills, five had bright red bills with black tips, and 13 showed a variable amount of red, mainly on the lower mandible. 109 BRITISH BIRDS Greater variation was observed in the colouring of the feet and legs of both "adults" and "first-winter" birds. For about half the fresh specimens, various shades of "dull", "dark" or "brownish" red were recorded, while the remainder ranged through orange-red, coral, true scarlet and bright crimson. These differences appeared to be purely individual and showed no correlation with the stage of moult.

(c) Sex Because of internal decomposition, dehydration or damage, sex could not be certainly determined in 27 specimens. Of the remainder, 50 (including 13 "adults") were females and 34 (eight "adults") were males. In most the gonads were small to minute. However, six females in adult plumage and three in "first-winter" dress showed some signs of enlargement, with ovaries measuring 1-1.5 cm. along their longest axes and largest 1-2 mm. in diameter. It is interesting to note that 60% of the sample were females and three possible explanations exist: (i) that there is a similar dispropor­ tion in the sex ratio of the living population; (ii) that females were more susceptible to the destructive agent; or (iii) that the bulk of the males had already left on their northward journey when the malady struck. Cullen (1957) believed that males predominated on certain breeding grounds of the related ; and Lack (1954) has discussed the "general impression of the ornithologist . . . that male birds are rather commoner than females, which suggests that females have a heavier mortality". Thus, on general grounds, the first possibility seems less likely than the second. However, Lack thought that heavier mortality was attributable to such factors as predation of hen birds while incubating, rather than to any inherent weakness associated with the fact that, amongst birds, females are the hetero- gametic sex.

(d) Weight Among 15 "adult" specimens judged sufficiently fresh to give reliable results, weights ranged from 76 gm. to 118 gm. and averaged 97.8 gm.; one of the lightest birds (77.2 gm.) was a male found alive and weighed a few hours before it died. Fifty-one "first-winter", birds ranged from 79 gm. to 115.5 gm. and averaged 100.2 gm.; seven of these which were taken alive had weights varying from 91.5 gm. to ii4gm. Szczepski and Kozlowski (1953), who provide the only weights of normal Common Terns that I can trace in the literature, gave a range of 101-175 gm. for adult birds. If it is assumed that the mean lies about half-way between these figures, then the present series averaged about 25% lighter than normal breeding birds. no COMMON TERN MORTALITY IN SOUTH AFRICA (e) Internal condition of afflicted birds The differences in weight between sick and healthy birds are rather smaller than might have been expected on the basis of post-mortem examinations, since all specimens in this series showed extreme emaciation. There was a marked wastage of the breast muscles and a complete absence of the subdermal fat deposits that are laid down by some long-distance migrants before their journey north. Lungs, liver, kidney, spleen and heart appeared normal, but most specimens exhibited inflammation of the lower intestine. However, the most striking abnormality was a marked clouding of the airsacs and visceral mesenteries with a film of greyish-yellow exudate. According to Brandly (1959), a similar lesion is frequently observed in infections with pneumotropic strains of Newcastle Disease. Further similarities between Newcastle Disease and the present epizootic were the signs of prostration exhibited by afflicted birds and the existence of a profuse fluid diarrhoea. Similar symptoms were also observed by Beretzk (1959) in an epidemic which destroyed many hundreds of Mallards (Anas platyrhynchos) near Szeged, Hungary, in 1957.

(/) Virologkal findings These will form the subject of a separate publication, but I am indebted to Professor Kipps for permission to mention here that a virus similar to, but not identical with, that of Newcastle Disease was isolated from the specimens supplied to his laboratory. Endeavours to identify this virus (which is lethal for domestic chicks) were at first unsuccess­ ful, but it has recently been shown that it is neutralised by a serum prepared from a virus believed to have been responsible for an epidemic amongst (Rissa tridactyld) in Scotland. Dr. Becker found that he could infect chicks experimentally by injection or, less success­ fully, by placing the virus in their drinking water. There was, how­ ever, no direct passage of the disease from infected birds to healthy companions; nor was it possible to induce illness in experimentally infected Swift Tern chicks. On the basis of these observations, it seems possible that the infec­ tion may have been spread in nature as a result of the terns' habit of drinking and bathing at their roosting places, for which they usually seek out stretches of shallow stagnant water that rapidly become con­ taminated with their own excreta. These same stretches of water are generally frequented by numbers of sand plovers, notably the White- fronted (Charadrim marginatus); a special watch was kept for signs of illness amongst these birds, therefore, but none was detected.

DISCUSSION The malady which overtook lingering or overwintering Common in BRITISH BIRDS Terns on southern Cape coasts during 1961 had several interesting features. Firstly, there was its sudden and virtually simultaneous onset in the third week of April at all points along the considerable stretch of coastline (approximately 1,000 miles) covered by the observa­ tions. Secondly, there was the equally abrupt cessation of mortality during the second week of May. From these two facts it would appear that the disease spread rapidly and ran a short course, killing or conferring immunity on all susceptible birds within a matter of days. Thirdly, the virus appears to have been curiously host-specific, pro­ ducing illness in Common Terns and (probably) in the somewhat dis­ tantly related , but not in Arctic Terns, Swift Terns or White-fronted Sandplovers or the scavenging Black-backed Gulls and Cape Ravens. Fourthly, the disaster was remarkable for its severity, which may be judged from the fact that at least 1,300 birds are known to have died in four small areas alone. Population studies indicate that, in normal circumstances, the average annual mortality among different bird species varies from about 20% to 60% (Lack 1954, Gibb 1961). However, despite the fact that such substantial numbers die, most do so unnoticed, as Captain le Gras remarked. Thus, although the full extent of the mortality in this disaster cannot be assessed, the number of dead birds counted suggests that it must have been very high indeed. A basic question remains: what precipitated this spectacular epi­ zootic? Patently, no infection generates spontaneously, but must always be present amongst the population to a greater or lesser degree. It is known, for instance, that Newcastle Disease in a mild or sub­ clinical form may persist unrecognised amongst poultry flocks for years at a time (Brandly 1959). Because the clinical disease is most prevalent in autumn and winter it has been suggested (e.g. by F. R. Beaudette, see Brandly 1959) that obvious manifestations are pro­ voked by cold or adverse weather. In the present case, there is a suggestion (the Kittiwake disaster) that the virus responsible is endemic on the breeding and feeding grounds of various in the northern hemisphere. It is thus not impossible that terns suffering subclinical infections may bring the virus south with them on their autumn migration. There was, however, a long interval between the October arrival of these birds in "winter" quarters and the onset of the disease nearly six months later. In his discussion of the "pestes" or pandemic maladies which periodically overtake the guanays and other seafowl of the Humboldt current, Murphy (1936) pointed out that illness is most pronounced and mortality highest in years when abnormal oceanographic con­ ditions prevail, more specifically when the warm equatorial current

112 COMMON TERN MORTALITY IN SOUTH AFRICA "El Nino" displaces the colder waters normally washing the South American west coast. He suggested that, although various diseases, abnormal multiplication of endoparasites, etc., must play their part in these disasters, their ultimate source "lies in the change in the physical environment and a resultant malnutrition". Lovat was inclined to place a similar interpretation upon the results of the classic study of strongylosis in (summary in Lack 1954); and the idea implicit in the suggestion by Beaudette, quoted above, is not very different. It amounts to this: a minor infection, present in subclinical form, may assume epidemic proportions with high mortality if the host popula­ tion is under some form of stress. The same might occur if the causative agent itself underwent some mutation enhancing its virulence. However, it was with the first possibility in mind that enquiries were set afoot regarding local marine and meteorological conditions during- March and April 1961. In the first of these months phenomenal rains amounting to as much as five times the normal fell over the interior of the Cape, and the Weather Bureau (1961) stated that "as far as can be ascertained.,. such heavy precipitation simultaneously over such a large area of the Karoo (60,000 square miles) has never before been recorded". Good rains continued during April and flooded rivers carried large amounts of silt to the sea. Regarding marine conditions, Messrs. de Jager and Rand of the Division of Fisheries kindly informed me that officers of their research vessels operating off the west coast noted nothing unusual. However, for evidence that some abnormalities did exist in the south I am indebted to E. Middlemiss, who left Cape Town on 21st April on a sea journey to Durban, On that date, between Cape Town and False Bay, he saw the most extensive areas of "red water" he has ever encountered. The patches were well-defined and, off Camps Bay to Slangkop, were hardly more than a few hundred yards apart. "Red water", which appears intermittently off Cape coasts, is produced by the excessive multiplication of a dinoflagellate, which is normally present in small numbers in the plankton. The organisms contain a highly poisonous alkaloid and various marine animals, such as fish and crawfish, have occasionally been recorded as dying in some numbers during these "blooms". The phenomenon is known from several parts of the world and its exact causation is not understood, but it is often associated with atypical meteorological conditions. The possibility thus exists that the outbreak of "red water" may have been directly associated with the illness in the terns, or it may have been the cause or result of other circumstances producing a food shortage and precipitating disease. Unfortunately, these suggestions cannot be advanced in any but the most tentative form. They deal in phenomena which are little 113 BRITISH BIRDS understood and which have been hardly measured, if at all. Further­ more, the epi2ootic itself began and ended so abruptly as to leave no time for the development of adequate investigations before the dis­ appearance (on migration ?) of most of the surviving birds.

REFERENCES ANON. (1956): "African recoveries of birds ringed in Europe". Ostrich, 27: 185. (i960): "Recovery of tern ringed in Finland". Ostrich, 31: 34. AUSTIN, O. L. (1942): "The lifespan of the Common Tern (Sterna hirundo)". Bird- Banding, 13: 159-176. BERETZK, P. (1959): "Observed cases of birds' epidemies". Aquila, ft): 371-372. BRANDLY, C. A. (1959): "Newcastle Disease". In Diseases of Poultry, edited by H. E. Biester and L. H. Schwarte. Iowa State Univ. Press. CULLEN, J. M. (1957): "Plumage, age and mortality in the Arctic Tern". Bird Study, 4: 197-207. GIBB, J. A. (1961): "Bird populations". In The Biology and Comparative Physiology of Birds, edited by A. J. Marshall. New York and London. LACK, D. (1954): The Natural Regulation of Animal Numbers. Oxford. MCLACHLAN, G. R., and LIVERSIDGE, R. (1957): Roberts' Birds of South Africa. Cape Town. MURPHY, R. C. (1936): Oceanic Birds of South America. New York. NORDSTROM, G. (1961): "Der Vogelberingung in Finnland im Jahre 1959". Mem. Soc. Flora Fauna Fennica, 36: 32-106. PETERSON, R. T. (1947): A Field Guide to the Birds. Boston, Mass. SPENCER, R. (1961): "Report on bird-ringing for 1960". Brit. Birds, 54: 449-495. SZCZEPSKI, J. B., and KOZLOWSKI, P. (1953): Pomocni^e Tabele Ornitologic^ne. Warsaw. WEATHER BUREAU, Dept. of Transport, S.A. (1961): "Monthly weather report". March 1961. WITHERBY, H. F., JOURDAIN, F. C. R., TICEHURST, N. F., and TUCKER, B. W. (1941): The Handbook of British Birds. London. Vol. 5.

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