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The influence of food availability on breeding success of African penguins Spheniscus demersus at Robben Island, South Africa
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The influence of food availability on breeding success of African penguins Spheniscus demersus at Robben Island, South Africa Robert J.M. Crawforda,b,*, Peter J. Barhamc, Les G. Underhillb, Lynne J. Shannona, Janet C. Coetzeea, Bruce M. Dyera, T. Mario Leshorod, Leshia Upfolda a
Department of Environmental Affairs and Tourism, University of Cape Town, Marine and Coastal Management, Private Bag X2, Rogge Bay 8012, South Africa b Avian Demography Unit, Department of Statistical Sciences, University of Cape Town, Rondebosch 7701, South Africa c HH Wills Physics Laboratory, University of Bristol, Tyndall Avenue, Bristol BS8 1TL, UK d Robben Island Museum, Robben Island 7400, South Africa
A R T I C L E I N F O
A B S T R A C T
Article history:
From 1989 to 2004, the breeding success of African penguins Spheniscus demersus at Robben
Received 17 November 2005
Island, South Africa was significantly related to estimates of the abundance of both their
Received in revised form
main prey species, anchovy Engraulis encrasicolus and sardine Sardinops sagax, and to the
17 March 2006
combined biomass of these species. When the combined spawner biomass of fish prey
Accepted 29 March 2006
was less than 2 million ton, pairs fledged an average of 0.46 chicks annually. When it
Available online 8 June 2006
was above 2 million ton, annual breeding success had a mean value of 0.73 chicks per pair. Given previously estimated values of survival and age at first breeding, these levels of
Keywords:
breeding success are inadequate to sustain the African penguin population. With the
African penguin
higher level of breeding success, an equilibrium situation might be attained if adult sur-
Breeding success
vival could be increased by 6–7% per annum. Attempts to reduce mortality of penguins
Fishing
have included the collection, cleaning and return to the wild of oiled birds, culling of Cape
Food
fur seals Arctocephalus pusillus pusillus seen preying on penguins around breeding localities
Mortality
and control of the spread of disease. Management of the purse-seine fishery should ensure
Spheniscus demersus
adequate escapement of fish to maintain the combined biomass of anchovy and sardine above 2 million ton. The maintenance of suitable breeding habitat and removal of feral predators from breeding localities will also be important in improving breeding success. Ó 2006 Elsevier Ltd. All rights reserved.
1.
Introduction
The African penguin Spheniscus demersus is endemic to southern Africa where it breeds at 29 localities between central Namibia and Algoa Bay on South Africa’s south coast (Hockey et al., 2005). There was a large decrease in numbers of African
penguins during the 20th century, from 1.45 million birds in adult plumage at Dassen Island alone in 1910 (Shannon and Crawford, 1999) to about 0.2 million at all breeding localities of the species in 2000 (Hockey et al., 2005), of which 55,000 were at Dassen Island (Crawford et al., 2000). This led to classification of the species as Vulnerable (BirdLife International,
* Corresponding author: Tel.: +27 21 4023140; fax: +27 21 4217406. E-mail addresses: [email protected] (R.J.M. Crawford), [email protected] (P.J. Barham), [email protected] (L.G. Underhill), [email protected] (L.J. Shannon), [email protected] (J.C. Coetzee), [email protected] (B.M. Dyer), [email protected] (T.M. Leshoro), [email protected] (L. Upfold). 0006-3207/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2006.03.019
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2004). The decreases in the early part of the 20th century were primarily driven by excessive harvests of their eggs, which were terminated in 1967 (Shelton et al., 1984). In the latter part of the 20th century, other factors contributed to the decrease, including oiling and competition with increasing populations of Cape fur seals Arctocephalus pusillus pusillus for breeding space (Hockey et al., 2005). Purse-seine fisheries developed rapidly off South Africa and Namibia after World War II. They reduced availability of food to penguins, especially off Namibia following the collapse there of the stock of sardine (pilchard) Sardinops sagax (Crawford, 1998). Numbers of penguins breeding in southern Namibia dropped from 40,000 pairs in 1956 to about 1000 pairs in 2000 (Crawford et al., 2001). Off South Africa, anchovy Engraulis encrasicolus and sardine are the main prey of African penguins. They contributed 50– 90% by mass of their diet in six studies conducted between 1953 and 1992, and 83–85% by number of prey items eaten in two studies between 1977 and 1985 (references in Hockey et al. (2005)). Trends in regional populations of African penguins are related to long-term changes in the abundance and distribution of these two fish species (Crawford, 1998). From 1984 to 1989, during a period when sardine was increasing off South Africa (Barange et al., 1999), the breeding success of African penguins in Saldanha Bay was significantly related to the contribution of sardine to the diet (Adams et al., 1992). From 1989 to 1995, breeding success at Robben Island was significantly related to the biomass of anchovy (Crawford et al., 1999). Subsequently, the biomass of anchovy and sardine off South Africa more than doubled between the mid 1990s and 2001 (Barange et al., 2004), providing further contrast in information available to examine the influence of food availability on the breeding success of African penguins. Here, we report results obtained using this extended data set and consider the influence of food biomass on sustainability of the African penguin population. Breeding success was measured at Robben Island, which was re-colonized by penguins in 1983, after an absence there of 180 years. The colony grew rapidly from nine pairs in 1983 to 7200 pairs in 2002 (Du Toit et al., 2004). Most of the early growth of the colony was attributable to immigration (Crawford et al., 1999). Most spawning by anchovy and sardine takes place on the Agulhas Bank, to the southeast of Robben Island (Fig. 1), from August to February (Shelton, 1986; Hampton, 1987). Much ichthyoplankton is subsequently carried by currents to nursery areas for small fish that lie north of Robben Island (Shelton and Hutchings, 1982). Young-of-the-year migrate southwards along the west coast of South Africa from March until September, past Robben Island, to join shoals of mature fish over the Agulhas Bank (Crawford, 1980). At Robben Island, African penguins initiate breeding in January, with the number of nests peaking around May and tailing off after September (Crawford et al., 1999). The establishment of nests takes several weeks and incubation lasts about 40 days (Randall, 1989). Hence, chicks are fed during that part of the year when young anchovy and sardine are migrating past the colony. Off western South Africa, the foraging range of penguins that are feeding chicks is estimated to be 11–28 km (Wilson et al., 1989; Petersen et al., 2005); on the south coast birds feed up to 40 km from their breeding locality (Heath and Randall, 1989).
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Fig. 1 – A schematic diagram of the spawning grounds, northward transport of ichthyoplankton and southward movement of young-of the-year of anchovy and sardine off South Africa, showing breeding localities of African penguins mentioned in the text (adapted from Crawford (1980)).
2.
Methods
Hydro-acoustic surveys to estimate the spawner biomass of anchovy and sardine off South Africa were conducted each year in November from 1984 to 2004. Similar surveys to estimate the abundance of young-of-the-year of these fish species were conducted in May. The surveys covered the known areas of spawning and recruitment. They consisted of a series of pre-stratified, randomly-spaced, parallel transects, designed to obtain estimates of stock size with known precision. The strata were predefined according to expected distribution patterns, based on early surveys (Barange et al., 1999). Methods used on the surveys have been described by Hampton (1987) and Barange et al. (1999). Published information on estimates of biomass (Hampton, 1987; Barange et al., 1999, 2004) was updated by records available to JCC. Breeding success of African penguins was measured at Robben Island for each year from 1989 to 2004. Methods used from 1989 to 2000 were the same as those described by Crawford et al. (1999). Breeding pairs were banded with stainlesssteel flipper bands and their nests marked at the start of the breeding season. Nests were subsequently monitored at twoweekly intervals throughout the main breeding period (February–October) because birds may replace clutches or raise two broods. Double-brooding was taken into account in estimating breeding success (Crawford et al., 1999). A chick was considered to have fledged if it reached the stage where more than half its body was covered with final fledgling plumage, i.e., when aged about 45 days or older (Seddon and van Heezik, 1993). Therefore, breeding success may be overestimated. From 2001 to 2004, a similar procedure was used, except that not all breeding pairs were banded with stainless-steel flipper bands. Some were banded with plastic flipper bands or left without bands. In these years the numbers of nests
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in each of the three categories were roughly equivalent. Again all nests were marked. Based on previous observations of pairs that had been banded, it was assumed that all eggs laid or chicks produced at nests where birds were not banded were attributable to a single pair. Earthwatch volunteers assisted with the monitoring, thereby enabling nests to be visited about once each week. The same nest sites, rather than the same individuals, were followed from year to year. However, because sites fell into disuse, it was necessary to add new nests each year to maintain adequate sample sizes. African penguins at Robben Island show relatively low fidelity to nest sites (Crawford et al., 1999). Therefore, it is not thought that there was a change over time in the ages of penguins monitored to measure breeding success. At the time of selection of some new nests breeding had been initiated, which may have led to breeding success being overestimated. In all years, nests were not considered to have been satisfactorily monitored if they were irregularly checked during the breeding period (e.g., because the nest marker had disappeared) or, to avoid inconsistent interpretation of breeding failure, if at the first time they were checked in a year they contained chicks older than recently-hatched chicks. Because larger chicks may wander from nests, those found at or near nests were only considered to have been produced at that nest if a chronological sequence could be observed, i.e., if there had earlier been eggs and small chicks at the nest. Most chicks tended to remain near nests until they had attained half their final fledgling plumage (pers. obs.). At more southern latitudes, flipper bands have been shown to have harmful effects on other species of penguin. However, in spite of the banding of large numbers of birds, there is no evidence that properly constructed and fitted bands have such effects on African penguins (Petersen and Branch, 2004). Correlation analysis was used to examine the relationship between breeding success and estimates of the biomass of spawners and young-of-the-year. In this analysis the year 2000 was excluded, because breeding was curtailed, after sinking of the Treasure on 23 June, by the oiling of more than 14,800 grown penguins at Robben Island, the removal from the island of a further 7000 grown penguins and the collection for rearing in captivity of some 2600 orphaned chicks (Crawford et al., 2000). The level of breeding success necessary to maintain a population of African penguins in equilibrium was estimated for different values of survival using the equation: B ¼ 2ð1 sa Þð1=sa Þ3 ð1=si Þ; where B = breeding success (chicks per pair per year), sa = the proportion of birds older than 1 year surviving in any year, and si = the proportion of birds surviving from fledging until 1 year of age. It was assumed that all African penguins breed for the first time when 4 years old and in every subsequent year that they are alive. Most breed for the first time when aged 4–5 years (Randall, 1983; Crawford et al., 1999; Whittington et al., 2005). The equation calculates the number of chicks that must fledge in order to replace the number of breeding adults that die. The factor 2 is included because it is pairs
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of birds that produce chicks. The proportion of adults dying each year is (1 sa). The terms (1/sa)3 and (1/si) are included to account for mortality between the ages of one and four (a period of 3 years) and from fledging to age one, respectively. Values used for sa were 0.81, 0.85, 0.87, 0.88 and 0.91. The value of 0.81 is the mean of estimates reported in the literature: 0.71 at St Croix Island from 1976 to 1982 (Randall, 1983), 0.71 at Dyer Island from 1979 to 1985 (La Cock and Ha¨nel, 1987), 0.82 at Robben Island from 1993 to 1994 (Crawford et al., 1999), 0.80 at Dassen Island and 0.82 at Robben Island from 1990 to 1999 (Whittington, 2002). The value of 0.91 is the maximum reported value (Randall, 1983). Values used for survival of birds in their first year were 0.43 and 0.51. The value of 0.43 is the mean of estimates reported in the literature: 0.32 at St Croix Island from 1976 to 1982 (Randall, 1983), 0.69 at Dyer Island from 1979 to 1985 (La Cock and Ha¨nel, 1987) and 0.31 at Robben Island and 0.38 at Dassen Island from 1987 to 1999 (Whittington, 2002). A value of 0.51 was used by Shannon and Crawford (1999).
3.
Results
Between 42 (1990, 1995) and 172 (2004) nests were deemed to have been successfully monitored each year (mean 91). Over 15 years from 1989 to 2004 (excluding 2000), the breeding success of African penguins at Robben Island varied between 0.32 (1990) and 0.97 (1997) chicks fledged per pair (Fig. 2). The overall mean, apportioning equal weight to years, was 0.62 (standard deviation 0.19). In 2000, breeding success was reduced to 0.23 chicks per pair by the Treasure oil spill. From 1989 to 1990 and 1993 to 1996, the combined spawner biomass of anchovy and sardine off South Africa was less than 2 million ton. In other years it was above this value (Fig. 2). The combined biomass of anchovy and sardine young-of-the-year was less than 0.5 million ton from 1989 to 1990 and in 1994 and 1996. It was between 0.5 and 1 million ton from 1991 to 1993, in 1995 and from 1997 to 1999. It was more than 1 million ton from 2000 to 2005 (Fig. 2). In years when the combined spawner biomass of anchovy and sardine was less than 2 million ton, the mean number of chicks fledged per pair was between 0.32 and 0.65 (mean 0.46). Excepting 2000, when biomass was above 2 million ton, breeding success ranged from 0.57 to 0.97 (mean 0.73) chicks per pair (Fig. 3). In years when the combined biomass of young-of-the year anchovy and sardine was less than 0.5 million ton, from 0.5 to 1 million ton and greater than 1 million ton (excluding 2000) the average breeding success was 0.46, 0.63 and 0.76 chicks per pair, respectively. When the year 2000 was excluded, the average number of chicks fledged per pair was significantly related to the spawner biomass of anchovy (r15 = 0.526, P < 0.05), sardine (r15 = 0.555, P < 0.05) and these two species combined (r15 = 0.591, P < 0.05). It was also significantly related to the young-of-the-year biomass of anchovy (r15 = 0.525, P < 0.05), sardine (r15 = 0.560, P < 0.05) and these two species combined (r15 = 0.546, P < 0.05). The best-fitting regression relating breeding success to the combined spawner biomass of anchovy and sardine was:
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Table 1 – Breeding success (chicks/pair/year) required to maintain a population of African penguins in equilibrium for different combinations of first-year and adult (birds older than 1 year) survival, assuming an age at first breeding of 4 years First-year survival
Adult survival
0.43 0.51 0.51 0.51 0.51
0.81 0.85 0.87 0.88 0.91
Breeding success 1.66 0.96 0.77 0.69 0.47
to 1.66 chicks per pair per year, depending on the values of survival used (Table 1).
Fig. 2 – Trends in the breeding success (chicks/pair) of African penguins at Robben Island (top) and in the biomass of spawning (centre) and young-of-the-year (bottom) anchovy, sardine and these two species combined, 1989–2004. The dashed line in the top panel indicates the mean breeding success during 1989–2004, excluding 2000 when the Treasure oil spill greatly decreased breeding success.
4.
Discussion
4.1.
Breeding success
In earlier studies, breeding success (chicks/pair/year) of African penguins was 0.37–0.67 at Dassen Island, 0.38 at St Croix Island, 0.63 in Saldanha Bay, 0.15–0.55 in Saldanha Bay and 0.61 at Boulders (references in Hockey et al. (2005)). These values have a range of 0.15–0.67, which spans that of 0.32–0.59 obtained at Robben Island from 1989 to 1995 (Crawford et al., 1999). In the present study it was found that, when the spawner biomass of anchovy and sardine was above 2 million ton, breeding success at Robben Island was 0.57–0.97 (mean 0.73) chicks per pair. Over 3 years, Humboldt penguins S. humboldti, which feed on anchoveta E. ringens, reared on average 4.54 fledglings, which equates to 1.51 chicks per pair per year (Paredes et al., 2002). Over 20 years, little penguins Euduptyla minor, for which sardine is a major constituent of the diet, had an average breeding success of 0.8 chicks fledged per pair (Dann and Cullen, 1990). These values are both greater than estimates of the average breeding success of African penguins, which eat similar prey.
4.2.
Fig. 3 – The relationship between the breeding success of African penguins (chicks/pair) and the combined spawner biomass of anchovy and sardine, 1989–2004, excluding 2000, when breeding was curtailed by the Treasure oil spill. The dashed line indicates the mean breeding success. The best-fitting regression curve is shown.
B ¼ 0:159ðln FÞ þ 0:461; where ln is the natural logarithm, and F = fish biomass. This regression has a r2 value of 0.382, indicating that it explained 38% of the variation in breeding success observed at Robben Island during 1989–2005. Estimates of breeding success required to maintain an African penguin population in equilibrium ranged from 0.47
Influence of food
The significant relationships obtained between breeding success of African penguins and estimates of the biomass of their fish prey confirm earlier observations that reproduction is influenced by the abundance of food (Adams et al., 1992; Crawford et al., 1999). In particular, except in 2000 when breeding was interrupted by an oil spill, breeding success improved markedly after the mid 1990s, coincident with a large increase in fish abundance (Fig. 2). From 1989 to 1995, the biomass of anchovy off South Africa was often much larger than that of sardine (Fig. 2) and breeding success of penguins was significantly related to the spawner biomass of anchovy (Crawford et al., 1999). Anchovy contributed most of the food of penguins at Robben Island from 1989 to 1992. After 1995, there was usually a high spawner biomass of sardine as well as of anchovy and, over the full period for which information is available (1989–2004), breeding success was related to the spawner biomass of both these
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fish species, as well as to their combined biomass. Breeding success was also related to the biomass of young-of-the-year anchovy and sardine, which pass the penguin colony at Robben Island before augmenting the spawning shoals of these fishes. When the spawner biomass of anchovy and sardine was above about 2 million ton, breeding success was generally high, but did not necessarily increase as biomass increased (Fig. 3), suggesting that there is a threshold biomass below which breeding success decreases. The abundance of food accounted for about 40% of the variation in breeding success observed between 1989 and 2004. Other factors, such as suitability of nesting habitat, also have an important impact. Excessive heat has caused abandonment of breeding attempts (Hockey et al., 2005). At Robben Island, feral cats Felis catus prey on eggs of African penguins (Crawford et al., 1999). Not only breeding success, but other factors such as absenteeism from breeding and age at first breeding also may be influenced by food availability. For example, from 1988 to 1995, the proportion of adults that nested at Robben Island was related to the spawner biomass of both anchovy and sardine (Crawford et al., 1999). The mean age of first breeding of African penguins in Namibia, where food is presently scarce, is 5–6 years (Whittington et al., 2005), compared to ages of 4–5 years reported for South Africa, where food is more plentiful (Randall, 1983; Crawford et al., 1999; Whittington et al., 2005). It is likely that a shortage of food will lead to reduced reproduction rates before it increases mortality (Cairns, 1987) but, in instances of extreme food shortage, other species of penguins have suffered high mortality through starvation (e.g., Hays, 1986; Valle and Coulter, 1987; Dann et al., 2000). Food has influenced breeding in other species of penguins. The 1982–83 El Nin˜o resulted in a scarcity of food off Peru and caused Humboldt penguins to abandon chicks in 1982 and not to breed in 1983 (Hays, 1986). Similarly, during the 1997–98 El Nin˜o, numbers of Humboldt penguins breeding at a colony in Chile decreased by more than 50% (Simeone et al., 2002). During the 1972 El Nin˜o there was almost complete breeding failure by Galapagos penguins S. mendiculus, thought attributable to reduced availability of food (Boersma, 1998). Little penguins bred about two weeks later than normal and fledged 0.3 chicks per pair compared with a long-term mean of 0.8, following a widespread mortality of sardine, one of their main food sources (Dann and Cullen, 1990; Dann et al., 2000). At Marion Island, the mass of chicks of macaroni penguins Eudyptes chrysolophus at fledging was significantly related to the contribution of fish to their diet (Crawford et al., 2003). At Be´chervaise Island, breeding success of Ade´lie penguins Pygoscelis adeliae decreased when adults had to forage farther from the colony and returned fewer or smaller meals to chicks (Irvine et al., 2000). At South Georgia, a four-fold decrease in biomass of Antarctic krill Euphausia superba led to a 90% decrease in breeding success of gentoo penguins P. papua (Croxall et al., 1999). Around the world stocks of anchovy and sardine have shown large fluctuations in their abundance (Schwartzlose et al., 1999). Troughs in abundance, when poor reproduction by penguins can be expected, may be deepened and extended by over-fishing (Schwartzlose et al., 1999). The influence of
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long-term changes, or regimes, in the distribution and abundance of anchovy and sardine on African penguins has been considered by Crawford (1998).
4.3.
Sufficient breeding
The relationship between breeding success of African penguins and the abundance of their prey suggests the possibility of managing the South African purse-seine fishery so as to ensure adequate escapement of fish for sufficient breeding by the penguins. The required breeding success will depend on the target population level for African penguins, a matter considered by Crawford (2004). Here, we restrict discussion to the target of maintaining the population at its present level. Given assumptions of an age at first breeding of 4 years, that penguins breed in each subsequent year and that the mean estimates of survival measured to date (0.43 in the first year, 0.81 thereafter) are applicable, it would be necessary for pairs to fledge 1.66 chicks per year on average to maintain the population in equilibrium (Table 1). This is much more than was measured at Robben Island in any year between 1989 and 2004. The situation is worsened by the fact that African penguins may not breed each year. At Robben Island from 1988 to 1995, the proportion of adults that nested in any year varied from 0.7 to 1.0 (Crawford et al., 1999). At Stony Point from 1982 to 1986 and 1989 to 1996, 20% of the possible number of breeding attempts were skipped (Whittington et al., 1996). Further, for a species that breeds monogamously, if all birds are to breed it is necessary that there be equal numbers of each sex and this may not be the case. However, 125 females and 112 males were collected at sea during 1954– 1956 (Rand, 1960), a ratio approximating parity. When first-year survival is increased to 0.51 and the survival of older birds is also increased, the required breeding success reduces (Table 1). For an adult survival of 0.85, a production of 0.96 chicks per pair is required for equilibrium, similar to the highest value yet measured (0.97 at Robben Island in 1997). If adult survival is 0.87, 0.77 chicks per pair are needed. If it is 0.88, 0.69 chicks per pair are required. These values approximate the mean production of 0.73 chicks per pair measured when the combined spawner biomass of anchovy and sardine was more than 2 million ton. If adult survival is 0.91, pairs must fledge on average 0.47 chicks each year, similar to the average of 0.46 for years when the overall spawner biomass was less than 2 million ton. These latter scenarios are optimistic given the most recent estimates of annual survival of adults of 0.80– 0.82 for the two most populous colonies of African penguins (Whittington, 2002). However, if adult survival can be enhanced by 6–7%, levels of breeding success attained when the overall biomass of spawning fish exceeds 2 million ton should be adequate to maintain the population. This highlights the need to minimize mortality.
4.4.
Limiting mortality
Mortality of African penguins is heightened by several factors including oiling, predation by seals and disease. Survival of adult birds at Robben Island decreased from 0.82 in 1993–94 to 0.75 in 1994–95, following oiling of penguins there in the
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Apollo Sea spill (Crawford et al., 1999). Advances made in the transport of oiled birds to rescue facilities and their care at these facilities has substantially decreased, but not eliminated, mortality caused by oiling (Whittington, 1999; Crawford et al., 2000). Over a period of 12 months during 1995–1996, Cape fur seals killed 842 African penguins (8.7% of the population) at Dyer Island (Marks et al., 1997). At Lambert’s Bay, seals kill 4% of adult penguins annually (Crawford et al., 2001). Culling of seals to reduce non-sustainable levels of predation on seabirds around their breeding localities has been advocated and implemented (David et al., 2003). Avian cholera Pasteurella multocida has caused high mortality of Cape cormorants Phalacrocorax capensis and mortality of African penguins in South Africa (Crawford et al., 1992). Carcases of birds dying from this disease have been burnt in attempts to restrict its spread (L. Waller, Cape Nature, pers. comm.). There is a need to reduce mortality of African penguins to the extent possible. However, for the conservation of the species, it is clearly also important to ensure an adequate availability of food so that reproduction by penguins is sufficient to offset mortality.
Acknowledgements Monitoring of nests at Robben Island from 2001 to 2004 was conducted during the course of a project of the Earthwatch Institute. We thank the Darwin Initiative and the Earthwatch Institute for funding the project and the many Earthwatch volunteers who participated in the collection of information. We are also grateful to all who assisted with monitoring nests during 1989–2000. We thank our research institutes (listed under addresses) and the National Research Foundation for supporting this research. The Robben Island Museum provided logistical support for our research. This paper is a contribution to the project on top predators (LMR/EAF/03/02) of the Benguela Current Large Marine Ecosystem (BCLME) Programme.
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Adams, N.J., Seddon, P.J., van Heezik, Y.M., 1992. Monitoring of seabirds in the Benguela upwelling system: can seabirds be used as indicators and predictors of change in the marine environment? South African Journal of Marine Science 12, 959–974. Barange, M., Hampton, I., Roel, B.A., 1999. Trends in abundance and distribution of anchovy and sardine on the South African continental shelf in the 1990s, deduced from acoustic surveys. South African Journal of Marine Science 21, 367–391. Barange, M., Coetzee, J.C., Twatwa, N.M., 2004. Strategies of space occupation by anchovy and sardine in the southern Benguela: the role of stock size and intra-species competition. ICES Journal of Marine Science 62, 645–654. BirdLife International, 2004. Threatened Birds of the World 2004. CD Rom version. BirdLife International, Cambridge, UK. Boersma, P.D., 1998. Population trends of the Gala´pagos penguin: impacts of El Nin˜o and La Nin˜a. The Condor 100, 245–253. Cairns, D.K., 1987. Seabirds as indicators of marine food supplies. Biological Oceanography 5, 261–271.
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Crawford, R.J.M., 1980. Seasonal patterns in South Africa’s Western Cape purse-seine fishery. Journal of Fish Biology 16, 649–664. Crawford, R.J.M., 1998. Responses of African penguins to regime changes of sardine and anchovy in the Benguela system. South African Journal of Marine Science 19, 355–364. Crawford, R.J.M., 2004. Accounting for food requirements of seabirds in fisheries management – the case of the South African purse-seine fishery. African Journal of Marine Science 26, 197–203. Crawford, R.J.M., Allwright, D.M., Hey¨l, C.W., 1992. High mortality of Cape cormorants (Phalacrocorax capensis) off western South Africa in 1991 caused by Pasteurella multocida. Colonial Waterbirds 15, 236–238. Crawford, R.J.M., Shannon, L.J., Whittington, P.A., 1999. Population dynamics of the African penguin Spheniscus demersus at Robben Island, South Africa. Marine Ornithology 27, 139–147. Crawford, R.J.M., Davis, S.A., Harding, R.T., Jackson, L.F., Leshoro, T.M., Mey¨er, M.A., Randall, R.M., Underhill, L.G., Upfold, L., van Dalsen, A.P., van der Merwe, E., Whittington, P.A., Williams, A.J., Wolfaardt, A.C., 2000. Initial impact of the Treasure oil spill on seabirds off western South Africa. South African Journal of Marine Science 22, 157–176. Crawford, R.J.M., David, J.H.M., Shannon, L.J., Kemper, J., Klages, N.T.W., Roux, J.-P., Underhill, L.G., Ward, V.L., Williams, A.J., Wolfaardt, A.C., 2001. African penguins as predators and prey – coping (or not) with change. South African Journal of Marine Science 23, 435–447. Crawford, R.J.M., Cooper, J., Dyer, B.M., 2003. Population of the macaroni penguin Eudyptes chrysolophus at Marion Island, 1994/95–2002/03, with information on breeding and diet. South African Journal of Marine Science 25, 475–486. Croxall, J.P., Reid, K., Prince, P.A., 1999. Diet, provisioning and productivity responses of marine predators to differences in availability of Antarctic krill. Marine Ecology Progress Series 177, 115–131. Dann, P., Cullen, J.M., 1990. Survival, patterns of reproduction, and lifetime reproductive output in little blue penguins Eudyptula minor on Phillip Island, Victoria, Australia. In: Davis, L.S., Darby, J.T. (Eds.), Penguin Biology. Academic Press, San Diego, pp. 63–84. Dann, P., Norman, F.I., Cullen, J.M., Neira, F.J., Chiaradia, A., 2000. Mortality and breeding failure of little penguins (Eudyptula minor) in Victoria, 1995–96, following a widespread mortality of pilchard (Sardinops sagax). Marine and Freshwater Research 51, 355–362. David, J.H.M., Cury, P., Crawford, R.J.M., Randall, R.M., Underhill, L.G., Mey¨er, M.A., 2003. Assessing conservation priorities in the Benguela ecosystem, South Africa: analysing predation by seals on threatened seabirds. Biological Conservation 114, 289–292. Du Toit, M., Underhill, L.G., Crawford, R.J.M., 2004. African Penguin Populations in the Western Cape, South Africa, 1992–2003. Avian Demography Unit, Cape Town. Hampton, I., 1987. Acoustic study on the abundance and distribution of anchovy spawners and recruits in South African waters. South African Journal of Marine Science 5, 901–917. Hays, C., 1986. Effects of the 1982–83 El Nin˜o on Humboldt penguin colonies in Peru. Biological Conservation 36, 169–180. Heath, R.G.M., Randall, R.M., 1989. Foraging ranges and movements of jackass penguins (Spheniscus demersus) established through radio telemetry. Journal of Zoology 217, 367–379. Hockey, P.A.R., Dean, W.R.J., Ryan, P.G. (Eds.), 2005. Roberts Birds of Southern Africa. Springer, seventh ed. John Voelcker Bird Book Fund, Cape Town. Irvine, L.G., Clarke, J.R., Kerry, K.R., 2000. Low breeding success of the Ade´lie penguin at Be´chervaise Island in the 1998/99 season. CCAMLR Science 7, 151–167.
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La Cock, G.D., Ha¨nel, C., 1987. Survival of African penguins Spheniscus demersus at Dyer Island, southern Cape, South Africa. Journal of Field Ornithology 58, 284–287. Marks, M.A., Brooke, R.K., Gildenhuys, A.M., 1997. Cape fur seal Arctocephalus pusillus predation on Cape cormorants Phalacrocorax capensis and other birds at Dyer Island, South Africa. Marine Ornithology 25, 9–12. Paredes, R., Zavalaga, C.B., Boness, D.J., 2002. Patterns of egg laying and breeding success in Humboldt penguins (Spheniscus humboldti) at Punta San Juan. Peru Auk 119, 244–250. Petersen, S.L., Branch, G.M., 2004. Penguin flipper banding and other forms of marking: workshop report. BirdLife South Africa, Cape Town. Petersen, S.L., Ryan, P.G., Gremillet, D., 2005. Is food availability limiting African penguins at Boulders?: a comparison of foraging effort at mainland and island colonies. Ibis 147, 14–26. Rand, R.W., 1960. The biology of guano-producing seabirds. 2. The distribution, abundance and feeding habits of the Cape penguin, Spheniscus demersus, off the south-western coast of the Cape Province. Investigational Report Sea Fisheries Research Institute South Africa 41, 1–28. Randall, R.M., 1983. Biology of the jackass penguin Spheniscus demersus (L.) at St. Croix Island, South Africa. Unpublished PhD Thesis, University of Port Elizabeth. Randall, R.M., 1989. Jackass penguins. In: Payne, A.I.L., Crawford, R.J.M. (Eds.), Oceans of Life off Southern Africa. Vlaeberg Publishers, Cape Town, pp. 244–256. Schwartzlose, R.A., Alheit, J., Bakun, A., Baumgartner, T.R., Cloete, R., Crawford, R.J.M., Fletcher, W.J., Green-Ruiz, Y., Hagen, E., Kawasaki, T., Lluch-Belda, D., Lluch-Cota, S.E., MacCall, A.D., Matsuura, Y., Nevarez-Martinez, M.O., Parrish, R.H., Roy, C., Serra, R., Shust, K.V., Ward, M.N., Zuzunaga, J.Z., 1999. Worldwide large-scale fluctuations of sardine and anchovy populations. South African Journal of Marine Science 21, 289–347. Seddon, P.J., van Heezik, Y.M., 1993. Behaviour of the jackass penguin chick. Ostrich 64, 8–12.
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Shannon, L.J., Crawford, R.J.M., 1999. Management of the African penguin Spheniscus demersus – insights from modelling. Marine Ornithology 27, 119–128. Shelton, P.A., 1986. Fish spawning strategies in the variable southern Benguela Current region. Unpublished PhD thesis, University of Cape Town. Shelton, P.A., Hutchings, L., 1982. Transport of anchovy, Engraulis capensis Gilchrist, eggs and early larvae by a frontal jet current. Journal du Conseil International pour l’Exploration de la Mer 40, 185–198. Shelton, P.A., Crawford, R.J.M., Cooper, J., Brooke, R.K., 1984. Distribution, population size and conservation of the jackass penguin Spheniscus demersus. South African Journal of Marine Science 2, 217–257. Simeone, A., Araya, B., Bernal, M., Diebold, N., Grzybowski, K., Michaels, M., Teare, J.A., Wallace, R.S., Willis, M.J., 2002. Oceanographic and climatic factors influencing breeding and colony attendance patterns of Humboldt penguins Spheniscus humboldti in central Chile. Marine Ecology Progress Series 227, 43–50. Valle, C.A., Coulter, M.C., 1987. Present status of the flightless cormorant, Galapagos penguin and greater flamingo populations in the Galapagos Islands, Ecuador, after the 1982– 83 El Nin˜o. The Condor 89, 276–281. Whittington, P.A., 1999. The contribution made by cleaning oiled African penguins Spheniscus demersus to population dynamics and conservation of the species. Marine Ornithology 27, 177–180. Whittington, P.A., 2002. Survival and movements of African penguins, especially after oiling. Unpublished PhD Thesis, University of Cape Town. Whittington, P.A., Hofmeyr, J.H., Cooper, J., 1996. Establishment, growth and conservation of a mainland colony of jackass penguins Spheniscus demersus at Stony Point, Betty’s Bay, South Africa. Ostrich 67, 144–150. Whittington, P.A., Klages, N.T.W., Crawford, R.J.M., Wolfaardt, A.C., Kemper, J., 2005. Age at first breeding in the African penguin. Ostrich 76, 14–20. Wilson, R.P., Nagy, K.A., Obst, B.S., 1989. Foraging ranges of penguins. Polar Record 25, 303–307.
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available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/biocon
The influence of food availability on breeding success of African penguins Spheniscus demersus at Robben Island, South Africa Robert J.M. Crawforda,b,*, Peter J. Barhamc, Les G. Underhillb, Lynne J. Shannona, Janet C. Coetzeea, Bruce M. Dyera, T. Mario Leshorod, Leshia Upfolda a
Department of Environmental Affairs and Tourism, University of Cape Town, Marine and Coastal Management, Private Bag X2, Rogge Bay 8012, South Africa b Avian Demography Unit, Department of Statistical Sciences, University of Cape Town, Rondebosch 7701, South Africa c HH Wills Physics Laboratory, University of Bristol, Tyndall Avenue, Bristol BS8 1TL, UK d Robben Island Museum, Robben Island 7400, South Africa
A R T I C L E I N F O
A B S T R A C T
Article history:
From 1989 to 2004, the breeding success of African penguins Spheniscus demersus at Robben
Received 17 November 2005
Island, South Africa was significantly related to estimates of the abundance of both their
Received in revised form
main prey species, anchovy Engraulis encrasicolus and sardine Sardinops sagax, and to the
17 March 2006
combined biomass of these species. When the combined spawner biomass of fish prey
Accepted 29 March 2006
was less than 2 million ton, pairs fledged an average of 0.46 chicks annually. When it
Available online 8 June 2006
was above 2 million ton, annual breeding success had a mean value of 0.73 chicks per pair. Given previously estimated values of survival and age at first breeding, these levels of
Keywords:
breeding success are inadequate to sustain the African penguin population. With the
African penguin
higher level of breeding success, an equilibrium situation might be attained if adult sur-
Breeding success
vival could be increased by 6–7% per annum. Attempts to reduce mortality of penguins
Fishing
have included the collection, cleaning and return to the wild of oiled birds, culling of Cape
Food
fur seals Arctocephalus pusillus pusillus seen preying on penguins around breeding localities
Mortality
and control of the spread of disease. Management of the purse-seine fishery should ensure
Spheniscus demersus
adequate escapement of fish to maintain the combined biomass of anchovy and sardine above 2 million ton. The maintenance of suitable breeding habitat and removal of feral predators from breeding localities will also be important in improving breeding success. Ó 2006 Elsevier Ltd. All rights reserved.
1.
Introduction
The African penguin Spheniscus demersus is endemic to southern Africa where it breeds at 29 localities between central Namibia and Algoa Bay on South Africa’s south coast (Hockey et al., 2005). There was a large decrease in numbers of African
penguins during the 20th century, from 1.45 million birds in adult plumage at Dassen Island alone in 1910 (Shannon and Crawford, 1999) to about 0.2 million at all breeding localities of the species in 2000 (Hockey et al., 2005), of which 55,000 were at Dassen Island (Crawford et al., 2000). This led to classification of the species as Vulnerable (BirdLife International,
* Corresponding author: Tel.: +27 21 4023140; fax: +27 21 4217406. E-mail addresses: [email protected] (R.J.M. Crawford), [email protected] (P.J. Barham), [email protected] (L.G. Underhill), [email protected] (L.J. Shannon), [email protected] (J.C. Coetzee), [email protected] (B.M. Dyer), [email protected] (T.M. Leshoro), [email protected] (L. Upfold). 0006-3207/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2006.03.019
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2004). The decreases in the early part of the 20th century were primarily driven by excessive harvests of their eggs, which were terminated in 1967 (Shelton et al., 1984). In the latter part of the 20th century, other factors contributed to the decrease, including oiling and competition with increasing populations of Cape fur seals Arctocephalus pusillus pusillus for breeding space (Hockey et al., 2005). Purse-seine fisheries developed rapidly off South Africa and Namibia after World War II. They reduced availability of food to penguins, especially off Namibia following the collapse there of the stock of sardine (pilchard) Sardinops sagax (Crawford, 1998). Numbers of penguins breeding in southern Namibia dropped from 40,000 pairs in 1956 to about 1000 pairs in 2000 (Crawford et al., 2001). Off South Africa, anchovy Engraulis encrasicolus and sardine are the main prey of African penguins. They contributed 50– 90% by mass of their diet in six studies conducted between 1953 and 1992, and 83–85% by number of prey items eaten in two studies between 1977 and 1985 (references in Hockey et al. (2005)). Trends in regional populations of African penguins are related to long-term changes in the abundance and distribution of these two fish species (Crawford, 1998). From 1984 to 1989, during a period when sardine was increasing off South Africa (Barange et al., 1999), the breeding success of African penguins in Saldanha Bay was significantly related to the contribution of sardine to the diet (Adams et al., 1992). From 1989 to 1995, breeding success at Robben Island was significantly related to the biomass of anchovy (Crawford et al., 1999). Subsequently, the biomass of anchovy and sardine off South Africa more than doubled between the mid 1990s and 2001 (Barange et al., 2004), providing further contrast in information available to examine the influence of food availability on the breeding success of African penguins. Here, we report results obtained using this extended data set and consider the influence of food biomass on sustainability of the African penguin population. Breeding success was measured at Robben Island, which was re-colonized by penguins in 1983, after an absence there of 180 years. The colony grew rapidly from nine pairs in 1983 to 7200 pairs in 2002 (Du Toit et al., 2004). Most of the early growth of the colony was attributable to immigration (Crawford et al., 1999). Most spawning by anchovy and sardine takes place on the Agulhas Bank, to the southeast of Robben Island (Fig. 1), from August to February (Shelton, 1986; Hampton, 1987). Much ichthyoplankton is subsequently carried by currents to nursery areas for small fish that lie north of Robben Island (Shelton and Hutchings, 1982). Young-of-the-year migrate southwards along the west coast of South Africa from March until September, past Robben Island, to join shoals of mature fish over the Agulhas Bank (Crawford, 1980). At Robben Island, African penguins initiate breeding in January, with the number of nests peaking around May and tailing off after September (Crawford et al., 1999). The establishment of nests takes several weeks and incubation lasts about 40 days (Randall, 1989). Hence, chicks are fed during that part of the year when young anchovy and sardine are migrating past the colony. Off western South Africa, the foraging range of penguins that are feeding chicks is estimated to be 11–28 km (Wilson et al., 1989; Petersen et al., 2005); on the south coast birds feed up to 40 km from their breeding locality (Heath and Randall, 1989).
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Fig. 1 – A schematic diagram of the spawning grounds, northward transport of ichthyoplankton and southward movement of young-of the-year of anchovy and sardine off South Africa, showing breeding localities of African penguins mentioned in the text (adapted from Crawford (1980)).
2.
Methods
Hydro-acoustic surveys to estimate the spawner biomass of anchovy and sardine off South Africa were conducted each year in November from 1984 to 2004. Similar surveys to estimate the abundance of young-of-the-year of these fish species were conducted in May. The surveys covered the known areas of spawning and recruitment. They consisted of a series of pre-stratified, randomly-spaced, parallel transects, designed to obtain estimates of stock size with known precision. The strata were predefined according to expected distribution patterns, based on early surveys (Barange et al., 1999). Methods used on the surveys have been described by Hampton (1987) and Barange et al. (1999). Published information on estimates of biomass (Hampton, 1987; Barange et al., 1999, 2004) was updated by records available to JCC. Breeding success of African penguins was measured at Robben Island for each year from 1989 to 2004. Methods used from 1989 to 2000 were the same as those described by Crawford et al. (1999). Breeding pairs were banded with stainlesssteel flipper bands and their nests marked at the start of the breeding season. Nests were subsequently monitored at twoweekly intervals throughout the main breeding period (February–October) because birds may replace clutches or raise two broods. Double-brooding was taken into account in estimating breeding success (Crawford et al., 1999). A chick was considered to have fledged if it reached the stage where more than half its body was covered with final fledgling plumage, i.e., when aged about 45 days or older (Seddon and van Heezik, 1993). Therefore, breeding success may be overestimated. From 2001 to 2004, a similar procedure was used, except that not all breeding pairs were banded with stainless-steel flipper bands. Some were banded with plastic flipper bands or left without bands. In these years the numbers of nests
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in each of the three categories were roughly equivalent. Again all nests were marked. Based on previous observations of pairs that had been banded, it was assumed that all eggs laid or chicks produced at nests where birds were not banded were attributable to a single pair. Earthwatch volunteers assisted with the monitoring, thereby enabling nests to be visited about once each week. The same nest sites, rather than the same individuals, were followed from year to year. However, because sites fell into disuse, it was necessary to add new nests each year to maintain adequate sample sizes. African penguins at Robben Island show relatively low fidelity to nest sites (Crawford et al., 1999). Therefore, it is not thought that there was a change over time in the ages of penguins monitored to measure breeding success. At the time of selection of some new nests breeding had been initiated, which may have led to breeding success being overestimated. In all years, nests were not considered to have been satisfactorily monitored if they were irregularly checked during the breeding period (e.g., because the nest marker had disappeared) or, to avoid inconsistent interpretation of breeding failure, if at the first time they were checked in a year they contained chicks older than recently-hatched chicks. Because larger chicks may wander from nests, those found at or near nests were only considered to have been produced at that nest if a chronological sequence could be observed, i.e., if there had earlier been eggs and small chicks at the nest. Most chicks tended to remain near nests until they had attained half their final fledgling plumage (pers. obs.). At more southern latitudes, flipper bands have been shown to have harmful effects on other species of penguin. However, in spite of the banding of large numbers of birds, there is no evidence that properly constructed and fitted bands have such effects on African penguins (Petersen and Branch, 2004). Correlation analysis was used to examine the relationship between breeding success and estimates of the biomass of spawners and young-of-the-year. In this analysis the year 2000 was excluded, because breeding was curtailed, after sinking of the Treasure on 23 June, by the oiling of more than 14,800 grown penguins at Robben Island, the removal from the island of a further 7000 grown penguins and the collection for rearing in captivity of some 2600 orphaned chicks (Crawford et al., 2000). The level of breeding success necessary to maintain a population of African penguins in equilibrium was estimated for different values of survival using the equation: B ¼ 2ð1 sa Þð1=sa Þ3 ð1=si Þ; where B = breeding success (chicks per pair per year), sa = the proportion of birds older than 1 year surviving in any year, and si = the proportion of birds surviving from fledging until 1 year of age. It was assumed that all African penguins breed for the first time when 4 years old and in every subsequent year that they are alive. Most breed for the first time when aged 4–5 years (Randall, 1983; Crawford et al., 1999; Whittington et al., 2005). The equation calculates the number of chicks that must fledge in order to replace the number of breeding adults that die. The factor 2 is included because it is pairs
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121
of birds that produce chicks. The proportion of adults dying each year is (1 sa). The terms (1/sa)3 and (1/si) are included to account for mortality between the ages of one and four (a period of 3 years) and from fledging to age one, respectively. Values used for sa were 0.81, 0.85, 0.87, 0.88 and 0.91. The value of 0.81 is the mean of estimates reported in the literature: 0.71 at St Croix Island from 1976 to 1982 (Randall, 1983), 0.71 at Dyer Island from 1979 to 1985 (La Cock and Ha¨nel, 1987), 0.82 at Robben Island from 1993 to 1994 (Crawford et al., 1999), 0.80 at Dassen Island and 0.82 at Robben Island from 1990 to 1999 (Whittington, 2002). The value of 0.91 is the maximum reported value (Randall, 1983). Values used for survival of birds in their first year were 0.43 and 0.51. The value of 0.43 is the mean of estimates reported in the literature: 0.32 at St Croix Island from 1976 to 1982 (Randall, 1983), 0.69 at Dyer Island from 1979 to 1985 (La Cock and Ha¨nel, 1987) and 0.31 at Robben Island and 0.38 at Dassen Island from 1987 to 1999 (Whittington, 2002). A value of 0.51 was used by Shannon and Crawford (1999).
3.
Results
Between 42 (1990, 1995) and 172 (2004) nests were deemed to have been successfully monitored each year (mean 91). Over 15 years from 1989 to 2004 (excluding 2000), the breeding success of African penguins at Robben Island varied between 0.32 (1990) and 0.97 (1997) chicks fledged per pair (Fig. 2). The overall mean, apportioning equal weight to years, was 0.62 (standard deviation 0.19). In 2000, breeding success was reduced to 0.23 chicks per pair by the Treasure oil spill. From 1989 to 1990 and 1993 to 1996, the combined spawner biomass of anchovy and sardine off South Africa was less than 2 million ton. In other years it was above this value (Fig. 2). The combined biomass of anchovy and sardine young-of-the-year was less than 0.5 million ton from 1989 to 1990 and in 1994 and 1996. It was between 0.5 and 1 million ton from 1991 to 1993, in 1995 and from 1997 to 1999. It was more than 1 million ton from 2000 to 2005 (Fig. 2). In years when the combined spawner biomass of anchovy and sardine was less than 2 million ton, the mean number of chicks fledged per pair was between 0.32 and 0.65 (mean 0.46). Excepting 2000, when biomass was above 2 million ton, breeding success ranged from 0.57 to 0.97 (mean 0.73) chicks per pair (Fig. 3). In years when the combined biomass of young-of-the year anchovy and sardine was less than 0.5 million ton, from 0.5 to 1 million ton and greater than 1 million ton (excluding 2000) the average breeding success was 0.46, 0.63 and 0.76 chicks per pair, respectively. When the year 2000 was excluded, the average number of chicks fledged per pair was significantly related to the spawner biomass of anchovy (r15 = 0.526, P < 0.05), sardine (r15 = 0.555, P < 0.05) and these two species combined (r15 = 0.591, P < 0.05). It was also significantly related to the young-of-the-year biomass of anchovy (r15 = 0.525, P < 0.05), sardine (r15 = 0.560, P < 0.05) and these two species combined (r15 = 0.546, P < 0.05). The best-fitting regression relating breeding success to the combined spawner biomass of anchovy and sardine was:
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Table 1 – Breeding success (chicks/pair/year) required to maintain a population of African penguins in equilibrium for different combinations of first-year and adult (birds older than 1 year) survival, assuming an age at first breeding of 4 years First-year survival
Adult survival
0.43 0.51 0.51 0.51 0.51
0.81 0.85 0.87 0.88 0.91
Breeding success 1.66 0.96 0.77 0.69 0.47
to 1.66 chicks per pair per year, depending on the values of survival used (Table 1).
Fig. 2 – Trends in the breeding success (chicks/pair) of African penguins at Robben Island (top) and in the biomass of spawning (centre) and young-of-the-year (bottom) anchovy, sardine and these two species combined, 1989–2004. The dashed line in the top panel indicates the mean breeding success during 1989–2004, excluding 2000 when the Treasure oil spill greatly decreased breeding success.
4.
Discussion
4.1.
Breeding success
In earlier studies, breeding success (chicks/pair/year) of African penguins was 0.37–0.67 at Dassen Island, 0.38 at St Croix Island, 0.63 in Saldanha Bay, 0.15–0.55 in Saldanha Bay and 0.61 at Boulders (references in Hockey et al. (2005)). These values have a range of 0.15–0.67, which spans that of 0.32–0.59 obtained at Robben Island from 1989 to 1995 (Crawford et al., 1999). In the present study it was found that, when the spawner biomass of anchovy and sardine was above 2 million ton, breeding success at Robben Island was 0.57–0.97 (mean 0.73) chicks per pair. Over 3 years, Humboldt penguins S. humboldti, which feed on anchoveta E. ringens, reared on average 4.54 fledglings, which equates to 1.51 chicks per pair per year (Paredes et al., 2002). Over 20 years, little penguins Euduptyla minor, for which sardine is a major constituent of the diet, had an average breeding success of 0.8 chicks fledged per pair (Dann and Cullen, 1990). These values are both greater than estimates of the average breeding success of African penguins, which eat similar prey.
4.2.
Fig. 3 – The relationship between the breeding success of African penguins (chicks/pair) and the combined spawner biomass of anchovy and sardine, 1989–2004, excluding 2000, when breeding was curtailed by the Treasure oil spill. The dashed line indicates the mean breeding success. The best-fitting regression curve is shown.
B ¼ 0:159ðln FÞ þ 0:461; where ln is the natural logarithm, and F = fish biomass. This regression has a r2 value of 0.382, indicating that it explained 38% of the variation in breeding success observed at Robben Island during 1989–2005. Estimates of breeding success required to maintain an African penguin population in equilibrium ranged from 0.47
Influence of food
The significant relationships obtained between breeding success of African penguins and estimates of the biomass of their fish prey confirm earlier observations that reproduction is influenced by the abundance of food (Adams et al., 1992; Crawford et al., 1999). In particular, except in 2000 when breeding was interrupted by an oil spill, breeding success improved markedly after the mid 1990s, coincident with a large increase in fish abundance (Fig. 2). From 1989 to 1995, the biomass of anchovy off South Africa was often much larger than that of sardine (Fig. 2) and breeding success of penguins was significantly related to the spawner biomass of anchovy (Crawford et al., 1999). Anchovy contributed most of the food of penguins at Robben Island from 1989 to 1992. After 1995, there was usually a high spawner biomass of sardine as well as of anchovy and, over the full period for which information is available (1989–2004), breeding success was related to the spawner biomass of both these
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fish species, as well as to their combined biomass. Breeding success was also related to the biomass of young-of-the-year anchovy and sardine, which pass the penguin colony at Robben Island before augmenting the spawning shoals of these fishes. When the spawner biomass of anchovy and sardine was above about 2 million ton, breeding success was generally high, but did not necessarily increase as biomass increased (Fig. 3), suggesting that there is a threshold biomass below which breeding success decreases. The abundance of food accounted for about 40% of the variation in breeding success observed between 1989 and 2004. Other factors, such as suitability of nesting habitat, also have an important impact. Excessive heat has caused abandonment of breeding attempts (Hockey et al., 2005). At Robben Island, feral cats Felis catus prey on eggs of African penguins (Crawford et al., 1999). Not only breeding success, but other factors such as absenteeism from breeding and age at first breeding also may be influenced by food availability. For example, from 1988 to 1995, the proportion of adults that nested at Robben Island was related to the spawner biomass of both anchovy and sardine (Crawford et al., 1999). The mean age of first breeding of African penguins in Namibia, where food is presently scarce, is 5–6 years (Whittington et al., 2005), compared to ages of 4–5 years reported for South Africa, where food is more plentiful (Randall, 1983; Crawford et al., 1999; Whittington et al., 2005). It is likely that a shortage of food will lead to reduced reproduction rates before it increases mortality (Cairns, 1987) but, in instances of extreme food shortage, other species of penguins have suffered high mortality through starvation (e.g., Hays, 1986; Valle and Coulter, 1987; Dann et al., 2000). Food has influenced breeding in other species of penguins. The 1982–83 El Nin˜o resulted in a scarcity of food off Peru and caused Humboldt penguins to abandon chicks in 1982 and not to breed in 1983 (Hays, 1986). Similarly, during the 1997–98 El Nin˜o, numbers of Humboldt penguins breeding at a colony in Chile decreased by more than 50% (Simeone et al., 2002). During the 1972 El Nin˜o there was almost complete breeding failure by Galapagos penguins S. mendiculus, thought attributable to reduced availability of food (Boersma, 1998). Little penguins bred about two weeks later than normal and fledged 0.3 chicks per pair compared with a long-term mean of 0.8, following a widespread mortality of sardine, one of their main food sources (Dann and Cullen, 1990; Dann et al., 2000). At Marion Island, the mass of chicks of macaroni penguins Eudyptes chrysolophus at fledging was significantly related to the contribution of fish to their diet (Crawford et al., 2003). At Be´chervaise Island, breeding success of Ade´lie penguins Pygoscelis adeliae decreased when adults had to forage farther from the colony and returned fewer or smaller meals to chicks (Irvine et al., 2000). At South Georgia, a four-fold decrease in biomass of Antarctic krill Euphausia superba led to a 90% decrease in breeding success of gentoo penguins P. papua (Croxall et al., 1999). Around the world stocks of anchovy and sardine have shown large fluctuations in their abundance (Schwartzlose et al., 1999). Troughs in abundance, when poor reproduction by penguins can be expected, may be deepened and extended by over-fishing (Schwartzlose et al., 1999). The influence of
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long-term changes, or regimes, in the distribution and abundance of anchovy and sardine on African penguins has been considered by Crawford (1998).
4.3.
Sufficient breeding
The relationship between breeding success of African penguins and the abundance of their prey suggests the possibility of managing the South African purse-seine fishery so as to ensure adequate escapement of fish for sufficient breeding by the penguins. The required breeding success will depend on the target population level for African penguins, a matter considered by Crawford (2004). Here, we restrict discussion to the target of maintaining the population at its present level. Given assumptions of an age at first breeding of 4 years, that penguins breed in each subsequent year and that the mean estimates of survival measured to date (0.43 in the first year, 0.81 thereafter) are applicable, it would be necessary for pairs to fledge 1.66 chicks per year on average to maintain the population in equilibrium (Table 1). This is much more than was measured at Robben Island in any year between 1989 and 2004. The situation is worsened by the fact that African penguins may not breed each year. At Robben Island from 1988 to 1995, the proportion of adults that nested in any year varied from 0.7 to 1.0 (Crawford et al., 1999). At Stony Point from 1982 to 1986 and 1989 to 1996, 20% of the possible number of breeding attempts were skipped (Whittington et al., 1996). Further, for a species that breeds monogamously, if all birds are to breed it is necessary that there be equal numbers of each sex and this may not be the case. However, 125 females and 112 males were collected at sea during 1954– 1956 (Rand, 1960), a ratio approximating parity. When first-year survival is increased to 0.51 and the survival of older birds is also increased, the required breeding success reduces (Table 1). For an adult survival of 0.85, a production of 0.96 chicks per pair is required for equilibrium, similar to the highest value yet measured (0.97 at Robben Island in 1997). If adult survival is 0.87, 0.77 chicks per pair are needed. If it is 0.88, 0.69 chicks per pair are required. These values approximate the mean production of 0.73 chicks per pair measured when the combined spawner biomass of anchovy and sardine was more than 2 million ton. If adult survival is 0.91, pairs must fledge on average 0.47 chicks each year, similar to the average of 0.46 for years when the overall spawner biomass was less than 2 million ton. These latter scenarios are optimistic given the most recent estimates of annual survival of adults of 0.80– 0.82 for the two most populous colonies of African penguins (Whittington, 2002). However, if adult survival can be enhanced by 6–7%, levels of breeding success attained when the overall biomass of spawning fish exceeds 2 million ton should be adequate to maintain the population. This highlights the need to minimize mortality.
4.4.
Limiting mortality
Mortality of African penguins is heightened by several factors including oiling, predation by seals and disease. Survival of adult birds at Robben Island decreased from 0.82 in 1993–94 to 0.75 in 1994–95, following oiling of penguins there in the
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Apollo Sea spill (Crawford et al., 1999). Advances made in the transport of oiled birds to rescue facilities and their care at these facilities has substantially decreased, but not eliminated, mortality caused by oiling (Whittington, 1999; Crawford et al., 2000). Over a period of 12 months during 1995–1996, Cape fur seals killed 842 African penguins (8.7% of the population) at Dyer Island (Marks et al., 1997). At Lambert’s Bay, seals kill 4% of adult penguins annually (Crawford et al., 2001). Culling of seals to reduce non-sustainable levels of predation on seabirds around their breeding localities has been advocated and implemented (David et al., 2003). Avian cholera Pasteurella multocida has caused high mortality of Cape cormorants Phalacrocorax capensis and mortality of African penguins in South Africa (Crawford et al., 1992). Carcases of birds dying from this disease have been burnt in attempts to restrict its spread (L. Waller, Cape Nature, pers. comm.). There is a need to reduce mortality of African penguins to the extent possible. However, for the conservation of the species, it is clearly also important to ensure an adequate availability of food so that reproduction by penguins is sufficient to offset mortality.
Acknowledgements Monitoring of nests at Robben Island from 2001 to 2004 was conducted during the course of a project of the Earthwatch Institute. We thank the Darwin Initiative and the Earthwatch Institute for funding the project and the many Earthwatch volunteers who participated in the collection of information. We are also grateful to all who assisted with monitoring nests during 1989–2000. We thank our research institutes (listed under addresses) and the National Research Foundation for supporting this research. The Robben Island Museum provided logistical support for our research. This paper is a contribution to the project on top predators (LMR/EAF/03/02) of the Benguela Current Large Marine Ecosystem (BCLME) Programme.
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