ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on March 5, 2007
ICES Journal of Marine Science: Journal du Conseil 2007 64(3):570-576; doi:10.1093/icesjms/fsm009
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An altered carrying capacity of the Benguela upwelling ecosystem for African penguins (Spheniscus demersus)
1 Department of Environmental Affairs and Tourism, Marine and Coastal Management, Private Bag X2, Rogge Bay 8012, South Africa
2 Avian Demography Unit, Department of Statistical Sciences, University of Cape Town, Rondebosch 7701, South Africa
Correspondence to R. J. M. Crawford: tel: +27-21-4023140; fax: +27-21-4217406; e-mail: crawford{at}deat.gov.za
Crawford, R. J. M., Underhill, L. G., Upfold, L., and Dyer, B. M. 2007. An altered carrying capacity of the Benguela upwelling ecosystem for African penguins (Spheniscus demersus). – ICES Journal of Marine Science, 64: 570–576.The carrying capacity of an ecosystem for a species is an input parameter that is required for some models that assess population viability. It may be changed by an altered structure or functioning of the ecosystem, e.g. as a consequence of changes brought about by fishing or environmental change. Hence, it cannot necessarily be assumed that the pristine level of abundance of a species reflects the present-day carrying capacity of the ecosystem for that species. Historical and modern information on abundance and density-dependent responses is used to investigate changes in the carrying capacity of the Benguela upwelling ecosystem for African penguins (Spheniscus demersus), a species categorized as vulnerable. The carrying capacity was estimated to decrease from 1.5–3.0 million adult birds in the 1920s to just 10–20% of this value from 1978 to 2006, as a result inter alia of increased competition for food with purse-seine fisheries and fur seals (Arctocephalus pusillus pusillus). From 1988/1989 to 2005/2006, the per capita recruitment of young penguins to a colony where nesting space was not limiting was inversely related to the size of that colony, suggestive of a density-dependent response perhaps related to food availability.
Keywords: African penguin, Arctocephalus pusillus pusillus, Cape fur seal, carrying capacity, density-dependence, fishing, food, recruitment, Spheniscus demersus
Received 1 November 2006; accepted 12 January 2007; advance access publication 5 March 2007.
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Introduction |
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The African penguin (Spheniscus demersus) is endemic to the Benguela upwelling ecosystem off southern Africa, which extends from southern Angola in the north to about Nelson Mandela Bay (Algoa Bay) in the east (Crawford et al., 2006b). The species currently breeds at 31 localities between Hollams Bird Island, central Namibia, and Bird Island, Nelson Mandela Bay (Figure 1; Hockey et al., 2005; Underhill et al., 2006). Its usual non-breeding range extends 3200 km around the southern African coast, from 18°S in Namibia to 29°S in KwaZulu-Natal. It occurs as a vagrant north to Sette Cama (2°32'S), Gabon, on the west African coast and to the Limpopo River mouth (25°S), Mozambique, on the east coast (Hockey et al., 2005).
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The African penguin is classified as vulnerable, following a large decrease in numbers during the 20th century (BirdLife International, 2004). There were
570 000 pairs at Dassen Island in 1930 (Shannon and Crawford, 1999). When the first survey of the species at all breeding localities was conducted in 1956, there were 140 000 breeding pairs in total (Rand, 1963a, b). In 2000, the overall population numbered 63 000 pairs (Hockey et al., 2005). In undertaking population viability assessments, individual-based models are frequently used to assess the probability of extinction of species or populations (Miller and Lacy, 2005). Such models often require the carrying capacity to be specified, usually the number of individuals of the species. Determining the carrying capacity is not straightforward. For species with an unfavourable conservation status, there may have been large decreases in the size of populations so that, when the populations are at a low level, density-dependent responses are not readily detected. For example, there may be an abundance of breeding space. Nor, given that there may have been changes to the foodwebs in an ecosystem, can it necessarily be assumed that the size of the pristine population equates to the present-day carrying capacity of the ecosystem.
There were large changes in the structure and functioning of the Benguela ecosystem during the 20th century. Cape fur seals (Arctocephalus pusillus pusillus), which had been exploited to low levels of abundance by the end of the 19th century, increased rapidly in numbers (Butterworth et al., 1995). Commercial fisheries were initiated (Crawford et al., 1987). Between them, seals and the fisheries removed 2 million tonnes more fish and cephalopods from the Benguela ecosystem in the 1980s than they did in the 1930s. In this period, the consumption by seals rose from 0.1 to 1.0 million tonnes, and the harvest by man from some 0.01 to 1.3 million tonnes (Crawford et al., 1992). The diet of seals and the catch by fisheries overlap considerably with the diet of African penguins (Crawford et al., 1987; David, 1989; Hockey et al., 2005). Here, we explore how the carrying capacity of African penguins by the Benguela upwelling ecosystem may have changed during the 20th century.
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Methods |
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We estimated the number of breeding pairs of African penguins at Dassen Island, off western South Africa, in the period 1921–1931 by multiplying areas occupied by penguins by the densities of nests. We divided the island into three regions, with high and moderate densities of nests or no nests, using information in Kearton (1931) and our own observations of the distribution of penguins at the island made during the years 1988–2006. Kearton (1931, p. 185) first visited Dassen Island in 1921.
Kearton (1931, p. vii) stated "they [penguins] are so numerous that in places one can barely walk between their nesting-burrows, and it is no uncommon thing for two pairs of nesting penguins to find themselves so crowded for space that their burrows run into each other. In the four square miles of the island there are six principal colonies—and each of them contains, at a rough estimate, three-quarters of a million penguins". Kearton (1931, p. 42) provided a sketch of the island showing the approximate locations of the six main colonies at that time. Except for the location of the colony at the centre of the island, they correspond to areas where penguin nests are concentrated today, so we delineated their borders using the current distributions. Subsequent to Kearton's visit, a low wall, completed by about 1942 (unpublished diary of D. B. Price, former inspector of Government Guano Islands, 1942), was built around Dassen Island, 100 m from the shoreline, to restrict penguins to the exterior of the island and thereby to facilitate the collection of penguin eggs (Rand, 1963a). The wall remained intact until 1991, when portions of it were removed to permit penguins to move easily to the interior of the island. We gauged the extent of the interior colony, from Kearton's (1931) map and the locations of expanses of flat rock and areas that are flooded during rains, where penguins could not have nested. Penguins today also nest in high densities in several smaller areas, so we assumed that they also did so between 1921 and 1931.
Kearton (1931, p. 45) stated "Except for the few patches of bare rock, the whole surface of the island is pitted with holes a few feet or less apart—the nesting burrows of penguins; indeed I doubt whether it would be possible, apart from those flat rocks, to find a single patch of thirty square yards that was bare of these nests or burrows. Every spot of earthy ground, every overhanging rock, every spot where tunnelling can be performed, is made use of, and late arrivals who are so unlucky as to find all the best places already occupied have to make what they can of shallow earth where it is possible to make only a slight indentation". We therefore assumed that areas with flat rocks were not used for nesting by penguins, and we delineated such areas using aerial photographs and ground observations. We also assumed that pans that fill with freshwater for a substantial portion of the year were not used. Areas not assigned as high-density or not used were assumed to have moderate densities of nests.
The extents of areas of high and moderate densities of nests were measured on an aerial photograph using an Ibas interactive image-analysis system. The photograph was scaled from ground measurements of straight edges of walls and buildings.
The density of penguin nest sites in November 1988 in areas of high and moderate densities of nests was determined. For each categorization of density, we counted the number of nest sites (both active and inactive) in 15 quadrants measuring 5 m x 5 m. The high-density measurements were made at Boom Point, West Bay, and Whale Bay (Figure 2), each of which was the locality of one of the main colonies noted by Kearton (1931). We attempted to select those areas having the highest densities of nests. The moderate density measurements were made at Boom Point, House Bay, and Waterloo Bay. We assumed that the mean densities obtained were applicable to the high-density and moderate-density areas of the period 1921–1931.
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At Robben Island, off western South Africa, we examined density-dependence in the number of African penguins recruiting to the island. There, we undertook counts of penguins in immature plumage in the feather-shedding phase of moult at approximately two-week intervals between October 1988 and June 2006 (Crawford et al., 2006c). African penguins moult from immature to adult plumage by
2 years of age (Randall, 1989). The feather-shedding phase (from the time the first feathers stand out until the last loose feathers fall away) has a mean duration of 12.7 days (s.d. = 1.4 days, n = 45; Randall et al., 1986). Counts were interpolated linearly to estimate numbers in moult for each day between actual counts (Underhill and Crawford, 1999). These interpolated counts were summed for the split year 1 July to 30 June, then divided by 12.7 to gauge the number of birds at Robben Island moulting in each split year. At Robben Island, moult is mainly from October to January (Underhill and Crawford, 1999). We took the number of immature birds moulting at the island to be the number of young birds recruiting to the island.
Counts of the number of pairs of penguins breeding at Robben Island were made each year during the main breeding season (February–July) from 1983, when the island was re-colonized (Crawford et al., 1995a), to 2006. The number of immature penguins (I) recruiting to the island in split year i/(i + 1) was related to the number of pairs of penguins (P) breeding at the island in year i – 1, when the immature birds would have fledged, using the model
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The overall number of young penguins recruiting to the island, as a function of the number of pairs at the island, was then calculated using the equation
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A colony will decrease when the number of recruits is fewer than the number of breeding adults that die (D), which we estimated as
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For other colonies of African penguins that were extant between 1978 and 2006, we assumed that the highest count of the number of breeding pairs represented the carrying capacity at that colony during that period. Information was updated from that published by Crawford et al. (1995b, 2001), Kemper et al. (2001), Hockey et al. (2005), and Underhill et al. (2006). At each colony that consisted of 1000 pairs or more, a count was conducted in at least 9 years (up to 24) (Table 1). Some small, remote colonies were accessed less often. The overall carrying capacity of the Benguela ecosystem was taken to be the sum of the carrying capacities at the individual colonies.
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Results |
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The estimated distribution of breeding African penguins at Dassen Island during the approximate period 1921–1931 is shown in Figure 2. The area occupied by the six main colonies described by Kearton (1931) was estimated to be 31 ha. Elsewhere on the island, it was estimated that penguins bred at high-density in an additional 5 ha, making a total of 36 ha. It was estimated that penguins bred in moderate densities over 145 ha of island.
In 1988, based on samples of size 15, the mean density of nest sites at Dassen Island was 0.72 nests m–2 (s.d. 0.07; range 0.64–0.88) in high-density areas, and 0.46 nests m–2 (s.d. 0.11; range 0.20–0.64) in moderate density areas. Using these values, it is estimated that 259 000 (s.d. 6500) pairs of penguins bred in the high-density areas and some 667 000 (s.d. 41 000) pairs elsewhere on the island. Hence, the estimated overall population at the island was 926 000 (s.d. 42 000) pairs, where only variations in nesting densities have been accounted for in calculating the standard deviation.
The number of African penguins breeding at Robben Island increased from nine pairs in 1983 (Crawford et al., 1995a) to 8500 pairs in 2004, before falling to 3700 pairs in 2006 (Figure 3). The numbers of adults moulting at the island peaked at 16000 birds in summer 2003/2004, and the numbers of immature birds peaked at 3000 from 2001/2002 to 2003/2004 (Figure 3).
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The number of immature penguins (I) recruiting to Robben Island was related to the number of pairs (P) breeding in the previous season by the expression
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8000 pairs (Figure 5). However, once mortality of breeding birds had been accounted for, the estimated carrying capacity for the island was 7700 pairs, 800 pairs fewer than the maximum number observed to breed at the island.
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The maximum counts of breeding penguins recorded at the 32 colonies of the species that were extant during the period 1978–2006 are shown in Table 1—the colony at North Reef is now extinct (Crawford et al., 2001). The largest colonies were about 25 000 pairs at Dassen Island, 23 000 pairs at Dyer Island, and 19 000 pairs at St Croix Island. At no other locality were there 10 000 pairs or more during this period. The sum of the maximum counts amounted to slightly more than 100 000 pairs.
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Discussion |
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At Robben Island during the period 1988–1993, based on counts of active nest sites and moulting birds, on average only 60% of African penguins in adult plumage (termed adults) bred in a given year (Crawford and Boonstra, 1994). Although African penguins moult to adult plumage by an age of some 2 years, they often only commence breeding when
4 years old (Randall, 1989; Crawford et al., 1995a, Whittington et al., 2005a). If it is assumed that at Dassen Island only 60% of adult penguins bred, the estimate of 926 000 (s.d. 42 000) pairs for the 1920s suggests a population then of 3 million (s.d. 140 000) adults. If space limitation caused a smaller proportion of adults to breed, the population would have been greater than this value. It is possible that nests were at higher densities from 1921 to 1931 than at the close of the 20th century, in which case the population then would also have been underestimated. Shannon and Crawford (1999) estimated, on the basis of egg harvests at Dassen Island and the exploitation rate that would have resulted in the observed decrease in these harvests, that there were 570 000 pairs and 1.45 million birds aged 2 years or more at the island in 1910. Westphal and Rowan (1971), also based on egg harvests, considered that there were 1.5 million penguins at the island from 1900 to 1930. The estimate derived here is somewhat higher than this, but substantially less than the estimates of 4.5–5 million penguins of Kearton (1931) and nine million penguins by a lighthouse-keeper (Shannon and Crawford, 1999).
Our estimate of the number of penguins at Dassen Island during the period 1921–1931 is particularly dependent on the extent of the area at Dassen Island where penguins were assumed to breed in moderate densities. Kearton (1931) roughly gauged that, outside the six main colonies, there were 500 000 penguins. If we add this value to our estimate for the numbers of penguins in high-density areas (863 000 adults), our overall estimate for the island reduces to about 1.4 million adults. If the other breeding localities of African penguins are also taken into consideration, it seems likely that the Benguela ecosystem in the early part of the 20th century supported some 1.5–3.0 million African penguins in total.
The method used to estimate the carrying capacity for Robben Island assumes that immature birds moulting at the island later breed there. First-breeding kittiwakes Rissa tridactyla tend to recruit to the previous year's most productive colonies and emigrate from the least-productive ones (Danchin et al., 1998). For guillemots Uria aalge, visiting birds form a substantial proportion of the immature population at a colony (Halley and Harris, 1993). Because most African penguins breed for the first time when aged 4 years (Whittington et al., 2005a), immature moulters will have another 2 years to select the locality where they will breed. Of more than 20 000 African penguins banded as chicks between 1978 and 1999, 14% settled to breed at non-natal colonies (Whittington et al., 2005b). However, of those banded off western South Africa and later re-sighted alive, there was no significant directional trend in their movements (Whittington et al., 2005c). This suggests that the number of immature birds moulting at Robben Island was a reasonable index of those recruiting there during the period under consideration.
A regional concordance in trends at African penguin colonies has been observed, colonies increasing in some regions, but decreasing in others (Crawford et al., 2001; Underhill et al., 2006). The emigration of first breeders is a mechanism whereby African penguins cope with an altered distribution of prey (Crawford, 1998). Hence, the summation of maximum counts obtained over the 29-year period 1978–2006 may overestimate the carrying capacity of the Benguela ecosystem. The carrying capacity estimated for Robben Island was about 90% of the maximum number of birds observed breeding there. However, when counts are made there may also be absenteeism of breeders (Randall et al., 1986). Therefore, it is thought likely that the carrying capacity of the Benguela ecosystem is currently of the order of 100 000 pairs or 300 000 birds aged 2 years or more, i.e. some 10–20% of the population in the 1920s. For Dassen Island, the present carrying capacity for penguins may be as low as 5% of that in the 1920s.
In theory, where the maximum sizes of fish are not available to seabirds, exploitation of such fish species may, by increasing production, increase the abundance of smaller fish and hence the availability of prey to seabirds (Furness, 2006). However, in the Benguela ecosystem, penguins are able to eat sardine (Sardinops sagax) and the smaller anchovy (Engraulis encrasicolus) at their maximum sizes. Sardine of length 21–25 cm were commonly eaten in the 1950s, with one fish of 29 cm being taken (Rand, 1960). These two fish are the main prey of African penguins (Hockey et al., 2005). The introduction of commercial purse-seine fisheries after World War II decreased the overall abundance of sardine and anchovy in the Benguela ecosystem (Crawford et al., 1987). The density of prey around penguin breeding localities will have decreased, lowering the carrying capacity of the ecosystem for penguins. Conversely, in the North Sea, the carrying capacity of the ecosystem for seabirds may have increased. A decreased abundance of predatory fish brought about by fishing may have led to an increase in the abundance of forage fish (Furness, 2002).
The increased population of fur seals will also have reduced the food available to African penguins. At present, other factors, such as oiling of birds and predation by Cape fur seals, through reducing survival (Crawford et al., 2001; Underhill et al., 2006), are also likely to be influencing the carrying capacity. Although space, and particularly competition with Cape fur seals for space (Shaughnessy, 1980, 1984; Crawford et al., 1989), limits the numbers of African penguins at some smaller colonies, this was not the case at any of the larger colonies during the period 1978–2006. However, it appears that space for nesting may have limited the penguin colony at Dassen Island in the early part of the 20th century (Kearton, 1931).
Cairns (1989) proposed that seabirds from neighbouring colonies typically occupy non-overlapping feeding zones, and that birds recruiting as first breeders choose the colony at which feeding conditions are most favourable. Investigation of isotopes in the blood of Magellanic penguins (S. magellanicus) has suggested that high densities of penguins at breeding colonies led to a depletion around colonies of high-quality prey items (Forero et al., 2002). A low density of food may recently have slowed the recruitment of first-breeding African penguins to the colony at Boulders (Petersen et al., 2005). The density-dependent response shown in this paper is further evidence that food in the vicinity of colonies may limit the recruitment of young African penguins.
Adults of several long-lived seabirds, including African penguins (Hockey et al., 2005), once breeding, show strong fidelity to partners and consequently return to the same breeding colonies, even though conditions at those colonies may have changed. For species displaying such life history characteristics, trends in the recruitment of first breeders to colonies present an opportunity to detect density-dependent responses. At colonies of northern gannets (Morus bassanus), per capita population growth rates decreased with increasing colony size, whereas mean foraging trip duration of breeding gannets was positively correlated with colony size (Lewis et al., 2001). There seemed to be net movement of young birds from big colonies to small ones (Moss et al., 2002). However, for Cape gannets (M. capensis) in the Benguela ecosystem, population growth rates are positively related to colony size, suggesting that environmental modulation of food supply is more important than density-dependent effects (Lewis et al., 2006). Trends in colonies of Cape gannets are related to long-term shifts in the distribution of prey species, indicating the potential of environmental change, as well as fishing, to modify the carrying capacity of ecosystems (Crawford et al., 2007). This will especially be the case if it places prey beyond the range of central-place foragers during their breeding season, but will also apply if the distribution of prey is altered such that it influences the condition of a predator at the onset of breeding (Crawford et al., 2006a). An altered distribution of prey, probably influenced by both environmental variability and fishing, led to severe decreases of African penguins in Namibia (Crawford et al., 2001).
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Acknowledgements |
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We thank our research institutes, South Africa's National Research Foundation, and the Earthwatch Institute for supporting this research. CapeNature, Department of Environmental Affairs and Tourism (South Africa), and Robben Island Museum provided logistical support. We thank J. Kemper for providing updated information on the numbers of African penguins in Namibia. This paper is a contribution to the project LMR/EAF/03/02 of the Benguela Current Large Marine Ecosystem (BCLME) Programme. The comments of two anonymous reviewers were much appreciated.
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