Sympatric species associations
I. Dolphinsnext section
Far more studies have been conducted of sympatric associations of dolphins than have been done on African apes (Table 2a, 2b). The dolphin studies, however, have been less systematic due to the difficulties of obtaining data in an aquatic medium. Therefore, ape-dolphin data are not always comparable. In this paper we seek parallels between the two groups, using parameters of evidence that seem appropriate for comparison (e.g., habitat use, diet, et cetera).
The regular presence of bottlenose dolphins along the coastline has made this dolphin one of the best-known cetaceans (e.g., Shark Bay, western Australia: Connor and Smolker, 1985; Connor et al., 1998; the Firth of Tay and Moray Firth, Scotland: Wilson et al., 1993, Wilson, 1995; Sarasota Bay, Florida: Scott et al., 1990; Wells, 1991; Argentine Bay: Würsig, 1978; Croatia, Mediterranean Sea: Bearzi et al., 1999; and in southern California: Weaver, 1987; Hansen, 1990; Weller, 1991; Defran et al., 1999, Bearzi 2005c). Some populations exhibit a fission-fusion grouping pattern where individuals associate in small groups that change more or less frequently in composition (Connor et al., 2000a).
Sympatric species of the genus Tursiops have been described by a few investigators (Table 2). Bottlenose dolphins and Indo-Pacific bottlenose dolphins (T. aduncus) appeared to be in direct sympatry around the Chinese waters of the Penghu archipelago and were frequently observed in mixed schools with other dolphin species (Yang, 1976; Zhou and Qian, 1985). These two species, however, differed ecologically: bottlenose dolphins preferred the coastal and shallow waters of the continental shelf feeding upon benthic or reef-dwelling fish and cephalopods whereas Indo-Pacific bottlenose dolphins favored offshore waters feeding mostly on schooling epipelagic and mesopelagic species (Wang et al., 2000).
In the Indian and western Pacific Oceans, Hale et al. (2000) recorded different preferences in habitat choice for the same species, with bottlenose dolphins frequenting both shallow waters and offshore reefs and Indo-Pacific bottlenose dolphins inhabiting estuaries and costal waters. This study showed that some areas were occupied exclusively by one species, with coastal regions of sympatry in their distribution.
Sympatric bottlenose dolphins and Indo-Pacific bottlenose dolphins also exist in south African waters (Wang et al., 2000), although Ross (1977) described these species as being typically allopatric. Ross (1977) noted different prey in their stomachs, with bottlenose dolphins exploiting deep reefs located offshore and Indo-Pacific bottlenose dolphins preferring shallow inshore waters.
Inshore populations of the genus Delphinus have been described for different areas worldwide, including California (Evans, 1975; Bearzi, 2005a), South Africa (Young and Cockroft, 1994), New Zealand (Neumann, 2001a and b) and the Mediterranean Sea (Bruno et al., 2004; Bearzi et al., 2005), whereas the ecology of offshore communities remains largely unknown (Evans, 1994). Short-beaked common dolphins (D. del-phis) and long-beaked common dolphins (D. capen-sis) occur sympatrically in tropical and temperate waters (Heyning and Perrin, 1994; Table 2a).
In Santa Monica Bay, California, the direct sympatric ecology of short-beaked common dolphins and long-beaked common dolphins was investigated (Bearzi, 2005a). Short-beaked common dolphins and long-beaked common dolphins were sympatric in the bay, but they were never seen in mixed schools (Bearzi, 2005a). The co-existence of these species is probably explained by an abundance of anchovies (Engraulis mordax), among their favorite food, and other prey in areas of local upwelling, as also reported by other authors (Mais, 1974; Evans, 1975; Hui, 1979). These sympatric species had similar diet (Fitch and Brownell, 1968), however, slight differences in their prey were observed (Schwartz et al., 1992). This difference in diet might indicate how partitioning of ecological niches may have reduced the occurrence of competition for food resources when the dolphins were in direct sympatry (Bearzi, 2003, 2005a).
In the same bay, the broad sympatric ecology of bottlenose dolphins, short-beaked common dolphins and long-beaked common dolphins was also investigated (Bearzi, 2005a). High abundance and year-round occurrence of the three species appeared to be correlated to prey abundance and, consequently, to the oceanography of this region (Bearzi, 2005a), as also reported for other small odontocetes in different locations (Cockcroft and Peddemors, 1990; Gowans and Whitehead, 1995; Defran et al., 1999). Eighty percent of bottlenose dolphin sightings (n = 157) were found in shallow waters and they were generally separated from the distribution of the two species of common dolphins showing spatial habitat partitioning (Bearzi, 2005a).
Das et al. (2000) reported slightly different dietary preferences for sympatric striped dolphins and short-beaked common dolphins in the north-east Atlantic (Bay of Biscay). In this area, both species were quite opportunistic feeders taking advantage of seasonally or locally abundant preys, but striped dolphins were observed displaying more opportunistic trophic habits compared to common dolphins (Das et al. 2000).
Habitat partitioning and direct sympatry have been observed for short-beaked common dolphins and other delphinids by Gowans and Whitehead (1995). These authors examined the summer distribution of short-beaked common dolphins, Atlantic white-sided dolphins (Lagenorhyncus acutus) and long-finned pilot whales (Globicephala melas) in the highly productive waters in and near a submarine canyon of the Scotian Shelf called the Gully. These species were much more abundant inside the Gully than outside, and they used some areas of the Gully slightly differently, showing spatial partitioning of habitat. Atlantic white-sided dolphins and short-beaked common dolphins divided the Gully temporally but not geographically whereas pilot whales ranged widely over the entire study site, preferring locations with flat relief.
Habitat partitioning and direct sympatry were observed for short-beaked common dolphins and bottlenose dolphins in the eastern Ionian Sea near the island of Kalamos (Politi et al., 1998; Bruno et al., 2004). The two sympatric species had adopted different foraging strategies, with common dolphins feeding in the water column or near the surface and bottlenose dolphins focusing on bottom prey (Ferretti et al., 1998). In spite of such sympatry, the two species rarely mixed and showed no direct interactions (Bearzi et al., 2005).
Frantzis and Herzing (2002) observed striped dolphins and short-beaked common dolphins also in mixed-species associations with Risso’s dolphins (Grampus griseus). Among the accountable factors for mixed-species associations in the Mediterranean Sea there were: 1) the relative abundance of each species, and 2) the potential dependence of common dolphins on striped dolphins when the former could not form single-species groups (Frantzis and Herzing, 2002).
Two forms of killer whales, resident and transient, are distinguished in the eastern north Pacific (Bigg, 1982; Baird and Dill, 1995). Residents and transients show differences in acoustics, morphology, pigmentation patterns, and genetics (Barrett-Lennard, Ford, and Heise, 1996; Ford et al., 1998; Baird, 2000). Besides significant differences, these populations are well known to live sympatrically (Table 2a).
In British Columbian and Washington waters, two communities of northern and southern resident killer whales live in broad sympatry with transient killer whales while displaying remarkable differences in feeding behaviour (Baird, 2000; Saulitis et al., 2000). Resident populations feed primarily on fish, while transient whales prey on marine mammals, mainly pinnipeds (Bigg et al., 1990; Ford et al., 1998; Saulitis et al., 2000). Bigg et al. (1990) and Ford et al. (1998) observed that resident killer whales of British Columbia, Washington and Alaska ate mostly salmonids, of which 50% were chinook (Oncorhynchus tshawytscha), the largest and most energy-rich species present year-round in these areas. Similarly, resident killer whales in Prince William Sound, Alaska, fed primarily on coho salmon (Oncorhynchus kisutch), while transient killer whales fed on harbour seals (Phoca vitulina) and Dall’s porpoises (Phocoenoides dalli; Saulitis et al., 2000).
In the various study areas, transients travel and forage more than residents (88.5-94.5% of their time vs. 58-72% of the time), whereas residents socialize and rest more than transients (Morton, 1990; Felleman et al., 1991; Baird, 1994; Saulitis et al., 2000). Saulitis et al. (2000) also reported that different prey choices among populations of killer whales were accompanied by different foraging strategies. Residents foraged in co-ordinated pods swimming at high speed, lunging, encircling and chasing fish at the surface (Similä and Ugarte, 1993; Barrett-Lennard et al., 1996); mammal-eating transients either swam along shorelines or in dispersed formation across open areas (Barrett-Lennard et al., 1996; Saulitis et al., 2000).
Baird and Dill (1995) found high variability in habitat use between resident and transient whales, with transient animals spending far more time in shallow waters. Dissimilarities existed also in diving patterns of these populations, with resident animals spending most of their time in the upper twenty metres of the water column and feeding on salmonids and with transient animals displaying longer mean dive durations between 20-60 m (Bigg et al., 1990; Baird 1994, 2000).
Associations between transient and resident killer whales have rarely been seen (Morton, 1990; Baird and Dill, 1995; Barrett-Lennard et al., 1996). These populations do not associate, most likely because of their strikingly different diet (Ford et al., 1998; Saulitis et al., 2000).
II. African Apes
Chimpanzees live in fission-fusion polygynous societies in which members of a community form temporary foraging associations (parties) of varying sizes (Goodall, 1986). This flexible grouping pattern is thought to be a social adaptation to a reliance on patchily distributed fruit trees (Wrangham, 1977), although the energy value of particular fruits varies widely and may play an important role (Conklin-Brittain et al., 2006). Chimpanzee party size and composition varies widely among study sites (Boesch and Boesch-Achermann, 2000; Pruetz, 2006). Party size is thought to correlate with the size and distribution of fruit patches and with the presence of females with sexual swellings (Chapman et al., 1994; Anderson et al., 2005, 2006), but empirical tests that separate these influences are lacking and the relative influences may vary from site to site (te Bockhorst and Hogeweg, 1994). Chimpanzee communities vary in size from 20 to over 100, depending on the site (Nishida, 1979; Mitani and Watts, 1999). Females spend most of their time with their offspring, rarely joining large foraging parties (Goodall, 1986). Estrous females provide an exception to this pattern, being both highly sociable and strongly attractive to males. The chimpanzee diet is mainly ripe fruit (70% of the diet), but their diet includes leaves, shoots, buds, blossoms, seeds, nuts, bark, invertebrates, birds, eggs, honey and a number of mammal species (Wrangham, 1977; Goodall, 1986; Stanford, 1998). The Kasakela chimpanzees of Gombe National Park use at least 141 species of trees and plants (Wrangham, 1977). However, 95% of feeding time is spent on half of these food types, and foods are selected in proportion to their availability (Wrangham, 1977).
Gorillas occur across a wide range of habitat types, and their ecology varies accordingly (e.g, Robbins et al., 2006). Mountain gorillas (Gorilla gorilla beringei) from the Parc d’Volcans in the Virunga mountains of Rwanda feed primarily on perennially available foliage and other non seasonal foods (Watts, 1984). Fruit comprises a large percentage of western lowland gorilla diets. In Equatorial Guinea, 40% of the diet was composed of fruit (Jones and Sabater-Pi, 1971; Sabater-Pi and Groves, 1972; Sabater-Pi, 1977). In Cameroon, evidence of fruit was found in 50% of all fecal samples (Calvert, 1985). Studies in Gabon (Tutin and Fernandez, 1985, 1993; Rogers et al., 1988; Williamson, 1988; Rogers, Maisels et al., 1990; Williamson et al., 1990), the Central African Republic (Remis, 1997; Goldsmith, 1999) and the Republic of Congo (Nishihara, 1992, 1995) indicate a large proportion of fruit in the diet. Although large amounts of fruit are consumed during certain times of the year more than 90% of the fecal samples contain fiber and leaf fragments (Rogers and Williamson, 1987; Williamson, 1988) and in one study herbaceous material was eaten in equal amounts throughout the year (Goldsmith, 1999).
Gorilla ranging is strongly influenced by habitat and food availability. The day range of Karisoke gorillas is short; over a period of seventeen months a group traveled between 190 and 3,300 m per day (mean = 570 m; Watts, 1991). Watts found that the effect of group size on time spent feeding is small, which suggests that the costs of social foraging are low for mountain gorillas. Lowland gorillas travel much farther per day. Tutin (1996) found an overall mean day range in Lopé of 1.1 km/day, while Remis (1994) found a mean at Bai Hokou, Central African Republic, of 2.3 km/day. Differences between sites may be related to habitat and group size differences.
Lowland gorillas travel significantly farther during periods of fruit availability. Research in Lopé (Tutin, 1996) and at Bai Hokou (Remis, 1997; Goldsmith, 1999) demonstrates that daily ranging behaviour is influenced by the degree of frugivory. Tutin et al. (1992) suggest that due to their reliance on terrestrial herbaceous vegetation, western lowland gorilla groups do not experience high levels of within-group feeding competition. As a result, they do not need to modify their group size, explaining why their grouping pattern resembled that of mountain gorillas. At Bai Hokou, however, there was a significant positive relationship between group size and daily path length during all seasons, suggesting high levels of within-group feeding competition. In addition, groups were found to form temporary subgroups that fed and slept separately from one another, perhaps as a way of reducing feeding competition (Remis, 1994; Goldsmith, 1999).
Mountain gorilla group size does not seem to influence day range either due to the widespread, abundant foliage on which they feed (Watts, 1996). Mountain gorillas live in relatively stable groups, and a variable number of offspring. Both male and female mountain gorillas tend to emigrate from their natal groups (Harcourt, 1978). Emigrating males either join all-male bands or travel by themselves; females either join a new breeding group or take up with a solitary male (Stewart and Harcourt, 1987). Harcourt et al. (1981) reported that 60% of studied groups at Karisoke had only one adult male. Approximately 10% of the groups were all-male bands (Stewart and Harcourt, 1987). An emerging picture of lowland gorilla social organization is of less cohesive groups that are more likely to contain multiple silverbacks (Tutin et al., 1992; Remis, 1994; Olejniczak, 1996; Goldsmith, 1999). Evidence from Lopé (Tutin et al., 1992), the Ndoki (Olejniczak, 1996), and Bai Hokou (Goldsmith, 1999) suggest a mean group size of about 9.5 individuals, with groups not exceeding 18 individuals. Average group size is larger in eastern lowland gorillas (G. g. graueri) (10.8; Yamagiwa and Basabose, 2006).
There are a small but growing number of detailed ecological studies of sympatric chimpanzee and gorilla populations (Table 2b). Jones and Sabater-Pi (1971) identified several means of ecological separation between the two species in Equatorial Guinea. During the wet season, gorillas ranged in fairly open areas of regenerating vegetation, while chimpanzees utilized the upper strata of primary forest. During the dry season, gorillas were found in dense vegetation at the edge of forests and occasionally in primary forest adjacent to areas of regenerating vegetation, while chimpanzees ranged mainly in the lower strata and on the ground in primary forest. The gorillas in Jones’ and Sabater-Pi’s study were reported to feed almost completely terrestrially, whereas chimpanzees were mostly arboreal feeders.
More detailed sympatric ecological studies have been conducted in the Lopé Reserve in Gabon, where chimpanzees and gorillas live at similar population densities (Tutin and Fernandez, 1985, 1993). Lowland gorilla diet at Lopé more closely resembles that of chimpanzees than that of mountain gorillas living in the Virungas (Rogers et al., 1990; Tutin and Fernandez, 1993). It appears that Lopé gorillas satisfy a substantial part of their energy needs from fruit, relying on leaves to provide protein (Rogers et al., 1990). Most gorilla plant foods (69%) are harvested arboreally (Tutin and Fernandez, 1993). Lopé chimpanzees consist of at least 174 food items in their diet, including 111 species of fruit (Tutin and Fernandez, 1993). Approximately 76% of Lopé chimpanzee plant foods are harvested arboreally (Tutin and Fernandez, 1993). There is great overlap in the diets of chimpanzees and gorillas at Lopé with approximately 60-80% of foods being eaten by both species (Williamson et al., 1990; Tutin and Fernandez, 1993). Gorillas are more likely to feed on terrestrial herbaceous vegetation than chimpanzees and are more ready than chimpanzees to concentrate on this vegetation when fruit is scarce. Chimpanzee and gorilla diets diverge most when fruit is not abundant, although it is mainly gorillas that shift foraging strategies while chimpanzees continue to forage extensively for ripe fruit even in periods of low fruit availability (Williamson et al., 1990; Remis, 1997). Direct interspecific interference competition has never been observed.
Research on sympatric gorillas and chimpanzees in the Nouabalé-Ndoki forest of the Congo and Central African Republic have revealed similar patterns of resource use. In Nouabalé-Ndoki, gorillas are more highly frugivorous than any other studied population (Kuroda, 1992; Nishihara, 1995). Their diet consists of over 63% fruit, which is consumed seasonally. Ndoki gorillas make extensive year-round use of swamp forest (Nishihara, 1995) and feed in fig trees in proximity to chimpanzees during times of fruit scarcity (Suzuki and Nishihara, 1992). They also feed extensively on aquatic herbaceous vegetation, perhaps as a fallback food analogous to the use of terrestrial herbaceous vegetation (Magliocca and Querouil, 1997).
Eastern lowland gorillas and chimpanzees are sympatric in Kahuzi-Biega National Park in eastern Democratic Republic of Congo (Yamagiwa et al., 1994; Yamagiwa et al., 1996). Gorillas occur there at a much higher density than chimpanzees. The higher population density of gorillas may have been related to the chimpanzee frugivorous diet in a mountainous area of low fruit diversity. Yamagiwa et al. (1996) found that gorillas ate a more diverse diet than chimpanzees did. Both species ate fruit over the entire annual cycle, though not necessarily the same species at the same time. They shared at least four important fruit species in their diets and both apes sometimes fed together in the same tree crown. Gorillas found at lower elevations in Kahuzi-Biega ate more fruit than those at higher elevations, apparently related to fruit availability differences (Yamagiwa et al., 1994). Ecologically, this population appears to be intermediate between western lowland and mountain gorilla populations in the degree of frugivory and the plant species diversity in the diet.
Results of the Bwindi Impenetrable Great Ape Project include the first detailed study of Bwindi gorilla feeding and ranging ecology (Nkurunungi, 2005) and preliminary information on Bwindi chimpanzee behavioural ecology (Stanford, 1999; Stanford and Nkurunungi, 2003). Bwindi gorilla diet is seasonally high in fruit; in some months more than 50% of gorilla dung samples contain seeds (Nkurunungi, 2005). In other months, however, the gorilla diet contains no fruit and is similar to the diet of gorillas in the Virungas (Watts, 1984; Stewart and Harcourt, 1987). Gorilla and chimpanzee diets are thus similar in some months, and chimpanzees range farther when fruit is scarce to find fruit. Day range is positively correlated with the percentage of fruit in the diet, although only slightly so. Bwindi gorillas are much more likely to construct nests in trees than their Virungas counterparts, who nest entirely on the ground (Nkurunungi, 2005).