MIGRATION STUDIES

The humpback whale is a truly cosmopolitan species, found in all oceans of the world (Clapham, Reference Clapham1997), and it is famous for its extensive migrations (Hoelzel, Reference Hoelzel1998). Humpback prey is relatively sparsely distributed in the tropics, so that individual cetaceans feeding in this habitat range over large areas in search for food. Prey of different types is abundant in boreal regions and polar regions where cold, nutrient rich waters are brought to the surface by upwellings (Hoelzel, Reference Hoelzel1998).

Several hypotheses have been proposed for these annual migrations: a vestigial behaviour from when the smaller ocean basins meant closer feeding and wintering areas; the optimization of energy budgets by breeding in warm water; increased calf (offspring) growth and survivorship in warm protected waters; and avoidance of killer whale (Orcinus orca) predation at low latitudes (Hoelzel, Reference Hoelzel1998; Rasmussen et al., Reference Rasmussen, Palacios, Calambokidis, Saborío, Rosa, Secchi, Steiger, Allen and Stone2007).

For humpback whales, breeding areas are at approximately 20° latitude in both hemispheres (Clapham & Mead, Reference Clapham and Mead1999), while the feeding areas are found in temperate to polar waters within the same hemisphere. Migratory timing varies with age, sex and reproductive status (Craig et al., Reference Craig, Herman, Gabriele and Pack2003). The first whales to leave the feeding areas and arrive to the breeding areas are lactating females with their calf from the previous year (yearling), followed by immature individuals, mature males, ‘resting’ females (those neither pregnant nor lactating) and lastly pregnant females. By the time they have to go back to their summer feeding grounds, and also as the winter breeding season progresses, the whales leave the breeding ground in reverse order: females with calves are the last to leave for summer feeding grounds (Dawbin, Reference Dawbin and Norris1966).

Humpback movement and migratory patterns can be studied by the comparison of photographs (photo-ID) of individually distinctive natural markings such as permanent scars or the pigment pattern on the ventral surface of the flukes, as well as comparison of their dorsal fin shape (Muñoz et al., Reference Muñoz, Félix, Flórez-González, Haase, Katona, Lodi, McOsker, Robertson, Stevick and Siciliano1998; Iwasaki & Kubo, Reference Iwasaki and Kubo2001; Stevick et al., Reference Stevick, De Godoy, Engel and Allen2006). The College of the Atlantic (Bar Harbor, Maine, USA) keeps the Antarctic Humpback Whale Catalogue and the North Atlantic Humpback Catalogue, which consists of a collection of identification photographs from throughout the southern hemisphere and North Atlantic, to identify re-sightings (Stevick et al., Reference Stevick, De Godoy, Engel and Allen2006). The great majority of humpbacks undertake the migration each year. However, a population of humpbacks in the Arabian Sea appears to remain in the region year-round, feeding and breeding in tropical waters but retaining a strongly seasonal breeding cycle (Clapham, Reference Clapham1998).

The individuals that are recorded in locations separated by hundreds or even thousands of miles give important information on patterns of movements, migration, and possible gene flow (Clapham, Reference Clapham1996). Studies based on photo-ID of tail pattern and coloration have identified individual humpbacks that have travelled approximately 5000 miles (about 8000 km) between their feeding and breeding grounds (see ‘Evidence of long movements’) (Clapham, Reference Clapham1997).

When migrating individuals are philopatric, returning to their natal breeding grounds, there is the potential for mixing of differentiated stocks in temporary assemblages on seasonal feeding grounds. This is one mechanism in which there can be genetically differentiated sympatric populations (Hoelzel, Reference Hoelzel1998).

For migratory cetacean stocks, there are a number of possible patterns of distribution and movement, depending on the species and the local environment. For example, primary movement may be between ‘private’ breeding and feeding grounds, with some possible movement across areas (Figure 1). In this case, stock structure may be expected to be apportioned between both feeding and breeding grounds (Hoelzel, Reference Hoelzel1998).

Fig. 1. Hypothetical migration from three populations. Complete arrows suggest primary and more probable movements between feeding and breeding areas. Dashed lines represent low-level secondary patterns of movement (Hoelzel, Reference Hoelzel1998, reproduced with permission).

The occurrence of multiple breeding stocks that converge on a single feeding area (Figure 2) is of great concern from the perspective of genetic conservation and management. In this case, differentiated breeding stocks mix in temporary assemblages, and the pattern of mixing can vary on both spatial and temporal scales. This could affect the differential impact of exploitation on the component stocks. For example, hunting in a given location for an extended period could result in takes from more than one stock as they move through the area (Hoelzel, Reference Hoelzel1998).

Fig. 2. Migrations from three hypothetical breeding grounds (A, B and C) to a unique feeding ground, represented by complete arrows. Return to non-natal breeding grounds is represented by dashed lines (only shown for population A) (Hoelzel, Reference Hoelzel1998, reproduced with permission).

GENETIC STUDIES

The observed seasonality in the whales' migration patterns results in a distribution called ‘antitropical’ (Davies, Reference Davies1962). This subject is crucial to the understanding of the genetic flow on whales, as when southern hemisphere humpbacks are in tropical waters (southern hemisphere winter), the northern hemisphere humpback whales are feeding at high latitudes (northern hemisphere summer). This situation reverses after 6 months, when the seasons invert. Consequently, there is always a vast geographical gap separating northern and southern whales (True, Reference True1904) and the effective interchange between northern and southern hemisphere populations is prevented, or limited, by the seasonal opposition of this migratory cycle (Baker et al., Reference Baker, Slade, Bannister, Abernethy, Weinrich, Lien, Urban, Corkeron, Calambokidis, Vasquez and Palumbi1994).

Also, in the northern hemisphere, where it is possible to find humpback whales in the Atlantic and in the Pacific Oceans, the movement between these populations is prevented by continental land masses (True, Reference True1904). In the southern hemisphere, humpback whales form a single circumpolar population distributed throughout the Southern Oceans (Mackintosh, Reference Mackintosh1965). Within each major oceanic population, humpback whales are thought to form relatively discrete subpopulations which are not separated by obvious geographical barriers (Chittleborough, Reference Chittleborough1965; Mackintosh, Reference Mackintosh1965; Katona & Beard, Reference Katona and Beard1990).

While feeding in high-latitude waters, the humpback populations are spread among several relatively discrete feeding stocks. In contrast, it is possible that whales from different feeding grounds mix on the same breeding grounds, and probably interbreed (Mattila et al., Reference Mattila, Clapham, Katona and Stone1989; Katona & Beard, Reference Katona and Beard1990).

However, little is known about the extent of nuclear gene flow in humpback whale populations. Due to land masses, direct movement between the North Atlantic and North Pacific populations is not possible (True, Reference True1904), but migration between hemispheres is less clear. Considering the assumption that whales do not like to swim in warmer water, unless they are in their breeding season, Davies (Reference Davies1962) proposed the theory that cross-equatorial dispersal was more frequent in the Pleistocene, when it is thought that the equator had cold water projections. However, photo-ID records prove that the equator is not an absolute geographical barrier (Stone et al., Reference Stone, Flórez-Gonzalez and Katona1990), but it is still not known for sure whether these animals seen in both hemispheres are rare exceptions to the rule, occasional visitors or proper breeding migrants (Valsecchi et al., Reference Valsecchi, Pasboll, Hale, Glockner-Ferrari, Ferrari, Clapahm, Larsen, Mattila, Sears, Sigurjonsson, Brown, Corkeron and Amos1997).

Inter-oceanic exchange is also expected to happen to some degree in the absence of geographical barriers, yet its documentation remains an exceptional event. Since only a modest degree of migration is sufficient to confound structure between populations, dispersal events may be rare and therefore hard to identify (Pomilla & Rosenbaum, Reference Pomilla and Rosembaum2005). Previous documentations of migrations of this scale have centred on trans-equatorial movements (Stone et al., Reference Stone, Flórez-Gonzalez and Katona1990; Rasmussen et al., Reference Rasmussen, Palacios, Calambokidis, Saborío, Rosa, Secchi, Steiger, Allen and Stone2007) and just a couple of inter-oceanic migrants have been previously identified by Chittleborough (Reference Chittleborough1965).

Although several statistical approaches permit an indirect estimate of gene flow between populations, it is often very difficult to distinguish between current exchange and retention of common ancestral genetic states, as both scenarios produce a similar pattern of allele sharing (Pomilla & Rosenbaum, Reference Pomilla and Rosembaum2005).

For species with sex-biased dispersal or philopatry, the population structure of genetic variation can be different for the maternally inherited mitochondrial genome and the biparentally inherited nuclear genome. The contrasting structure of this genetic variation can, in turn, reveal the complexity of mating systems and one-way or return dispersal in species where demographic evidence is difficult to obtain (Baker et al., Reference Baker, Medrano-González, Calambokidis, Perry, Pilcher, Rosenbaum, Straley, Urban-Ramirez, Yamaguchi and Von Ziegesar1998). The following genetic studies on humpback whales are based mainly on mitochondrial and nuclear DNA.

Mitochondrial DNA

Genetic studies of humpback whales based on mitochondrial DNA (mtDNA) analysis have shown that humpback whale populations are distributed into three principal oceanic populations: the North Atlantic, the North Pacific and the Southern Oceans (Baker et al., Reference Baker, Palumbi, Lambertsen, Weinrich, Calambokidis and O'Brien1990, Reference Baker, Gilbert, Weinrich, Lambertsen, Calambokidis, Mcardle, Chambers and ÓBrien1993, Reference Baker, Slade, Bannister, Abernethy, Weinrich, Lien, Urban, Corkeron, Calambokidis, Vasquez and Palumbi1994). Mixing between those regions is not seen very often, and is considered slight, although occasional exchanges, especially between the North Pacific breeding grounds have been reported (Valsecchi et al., Reference Valsecchi, Pasboll, Hale, Glockner-Ferrari, Ferrari, Clapahm, Larsen, Mattila, Sears, Sigurjonsson, Brown, Corkeron and Amos1997).

The Baker et al. (Reference Baker, Gilbert, Weinrich, Lambertsen, Calambokidis, Mcardle, Chambers and ÓBrien1993) study on mtDNA showed high levels of variation in humpback whales and substantial genetic differences between oceanic populations. High variation in extant populations would not be due to recent divergence or frequent oceanic interchange but to the persistence of the divergent humpback whale mtDNA lineages for millions of years. This study also calculated the minimum number of migration events necessary to explain the current geographical distribution of nucleotypes worldwide (further information and complete data in Baker et al., Reference Baker, Gilbert, Weinrich, Lambertsen, Calambokidis, Mcardle, Chambers and ÓBrien1993), which was found to be six. Of these, two have been from the Southern Oceans to the North Atlantic, two have been from the North Atlantic to the Southern Oceans, and two have been from the Southern Oceans to the North Pacific. The observations that humpback whales migrate from the Antarctic Peninsula to the equatorial coast of Colombia (Stone et al., Reference Stone, Flórez-Gonzalez and Katona1990) support the hypothesis that the Pacific coast of South America is a likely route for gene flow between oceans (Figure 3) (Baker et al., Reference Baker, Palumbi, Lambertsen, Weinrich, Calambokidis and O'Brien1990).

Fig. 3. Migratory destinations and population structure of humpback whales in the North Pacific and western North Atlantic Oceans, based on natural marked individuals recognized by photo-ID. Arrows connect seasonal habitats visited by individually identified whales but do not necessarily indicate migratory routes. Thick arrows connect regions with known strong migratory interchange and thin arrows connect regions with weak migratory interchange. The broken line connecting Hawaii and Mexico indicates the probable presence of an intervening seasonal migration to a feeding ground by individuals sighted on both winter grounds in alternate years (Baker et al., Reference Baker, Palumbi, Lambertsen, Weinrich, Calambokidis and O'Brien1990, reproduced with permission).

The Baker et al. (Reference Baker, Slade, Bannister, Abernethy, Weinrich, Lien, Urban, Corkeron, Calambokidis, Vasquez and Palumbi1994) study on the hierarchical structure of mtDNA gene flow among Megaptera novaeangliae worldwide demonstrated a high degree of geographical differentiation both within and between the three distinct oceanic populations of humpback whales, despite the nearly unlimited migratory potential of this species. Consequently, the analysis of mtDNA showed a striking degree of genetic structure within and among oceanic populations.

Humpback whales, as other cetacean species, have survived near-extinction after the massive hunting in the past without major loss of mtDNA variation. This apparent genetic diversity in humpback populations could be due to insufficient time since exploitation for the effects of drift to be measured (Baker et al., Reference Baker, Gilbert, Weinrich, Lambertsen, Calambokidis, Mcardle, Chambers and ÓBrien1993). Therefore, the long generation time and age structure of humpback whale populations may have allowed them to pass through a brief bottleneck without major loss of genetic variation (Nei et al., Reference Nei, Maruyama and Chakraborty1975).

Due to the tremendous mobility of humpback whales and the apparent absence of geographical barriers within ocean basins, the formation of significant genetic divisions between stocks indicates strong fidelity to migratory destinations, as a result of a calf's early maternally inherited experience (Baker et al., Reference Baker, Slade, Bannister, Abernethy, Weinrich, Lien, Urban, Corkeron, Calambokidis, Vasquez and Palumbi1994), especially in its first year of life (Baker et al., Reference Baker, Palumbi, Lambertsen, Weinrich, Calambokidis and O'Brien1990, Reference Baker, Medrano-González, Calambokidis, Perry, Pilcher, Rosenbaum, Straley, Urban-Ramirez, Yamaguchi and Von Ziegesar1998). The occasional ability of individual whales to visit alternative breeding grounds and, as sometimes seen, to move between feeding grounds argues against a strict behavioural imprinting or site-specific genetic programming underlying this fidelity. Instead, the life history of such whales suggests a likely mechanism for a ‘cultural’ transmission of migratory destinations (Baker et al., Reference Baker, Palumbi, Lambertsen, Weinrich, Calambokidis and O'Brien1990), as can be confirmed from the mtDNA analysis and its known maternal inheritance.

However, the results obtained from mtDNA analysis are only one genetic measure attributable to the segregation of maternal lineages. The observations of migratory interchange between breeding grounds suggest that the structure of nuclear DNA variation may be more complex (Baker et al., Reference Baker, Slade, Bannister, Abernethy, Weinrich, Lien, Urban, Corkeron, Calambokidis, Vasquez and Palumbi1994).

EVIDENCE OF LONG MOVEMENTS

There are reports of humpback whales migrating long distances, from their feeding to their breeding grounds, and also in the opposite direction (Rasmussen et al., Reference Rasmussen, Palacios, Calambokidis, Saborío, Rosa, Secchi, Steiger, Allen and Stone2007). Evidence on these migratory patterns is based on movements of individuals identified by natural markings as part of a large-scale international collaboration, with participation of several organizations (Stevick et al., Reference Stevick, Aguayo, Allen, Avila, Capella, Castro, Chater, Rosa, Engel, Félix, Flórex-González, Freitas, Haase, Llano, Lodi, Muñoz, Olavarría, Secchi, Sheidat and Siciliano2004). Trans-oceanic migration events appear to be very rare in humpback whales, but both Matthews (Reference Matthews1937) and Mackintosh (Reference Mackintosh1942) reported humpback whale catches near the equator during the austral winter off the western coasts of South America and Africa, and suggested that some southern hemisphere whales winter in areas north of the equator (Rasmussen et al., Reference Rasmussen, Palacios, Calambokidis, Saborío, Rosa, Secchi, Steiger, Allen and Stone2007). Chittleborough (Reference Chittleborough1965) also demonstrated that extensive movement across stocks occurs, as shown by the movement of marked whales from Western Australia into the South Pacific.

Considering the North Atlantic, animals which feed at sites off the United States, Canada and west Greenland migrate southward to Caribbean waters during the winter where mating probably takes place (Perkins et al., Reference Perkins, Bryant, Nichols and Patten1982; Whitehead et al., Reference Whitehead, Chu, Perkins, Bryant and Nichols1983). Photo-ID matches provide evidence that humpback whales from the Icelandic feeding grounds and those from feeding areas in the north-western Atlantic utilize a common breeding area and may thus interbreed. The Icelandic photographs that proved to match with Caribbean-photographed humpbacks suggest that there is a significant interchange of animals between these areas (number of recognized humpbacks = 3, mean migration distance = 5958 km) (Figure 3) (Martin et al., Reference Martin, Katona, Mattila, Hembree and Waters1984).

The migratory destinations of humpback whales from the Antarctic Peninsula feeding region and the breeding grounds off the coasts of South America are still uncertain. The number of individuals re-sighted in the Antarctic Peninsula differed dramatically between eastern and western South America. From the western South American humpback population, 43 individuals were identified (through photo-ID) off the Antarctic Peninsula. On the other hand, no animals from Brazil were re-sighted in either the Antarctic Peninsula or off western South America (Figure 4). This evidence suggests that the north-western coast of South America represents an important breeding ground destination for those whales that feed off the Antarctic Peninsula. However, no support concerning the movements of humpback whales between the Antarctic Peninsula and the east coast of South America is provided (Stevick et al., Reference Stevick, Aguayo, Allen, Avila, Capella, Castro, Chater, Rosa, Engel, Félix, Flórex-González, Freitas, Haase, Llano, Lodi, Muñoz, Olavarría, Secchi, Sheidat and Siciliano2004), suggesting that humpback whales from the north-eastern coast of South America probably feed in other regions of the Antarctic (Muñoz et al., Reference Muñoz, Félix, Flórez-González, Haase, Katona, Lodi, McOsker, Robertson, Stevick and Siciliano1998).

Fig. 4. Potential migratory destinations between the Antarctic Peninsula feeding grounds to the breeding grounds off South America. Arrows serve to connect potential migratory endpoints and are not intended to indicate routes of travel (Stevick et al., Reference Stevick, Aguayo, Allen, Avila, Capella, Castro, Chater, Rosa, Engel, Félix, Flórex-González, Freitas, Haase, Llano, Lodi, Muñoz, Olavarría, Secchi, Sheidat and Siciliano2004, reproduced with permission).

These findings were confirmed when humpback whales from the southern Pacific were sighted off Panama and Costa Rica in the austral winter as far north as 11°N using this area for calving and mating. Evidence of this long movement is a report of seven individuals, including a mother and a calf, who have travelled approximately 8300 km, from a wintering area off the Pacific coast of Central America to feeding areas off Antarctica. This movement is the longest ever taken by any mammal. These whales were observed as far north as 11°N off Costa Rica, in an area also used by a boreal population during the opposite winter season, resulting in unique spatial overlap between northern and southern hemisphere populations (Rasmussen et al., Reference Rasmussen, Palacios, Calambokidis, Saborío, Rosa, Secchi, Steiger, Allen and Stone2007).

Stone et al. (Reference Stone, Flórez-Gonzalez and Katona1990) also reported a humpback whale that has migrated from the Antarctic Peninsula to Colombia (8334 km according to Stone et al. (Reference Stone, Flórez-Gonzalez and Katona1990) and 7878 km according to Rasmussen et al. (Reference Rasmussen, Palacios, Calambokidis, Saborío, Rosa, Secchi, Steiger, Allen and Stone2007); the discrepancy is due to the methods that are utilized by each of the authors). Again, it is suggested that this whale probably belongs to a population that feeds in Antarctica and breeds off the coast of Colombia, giving interesting implications for the possibility of migration between hemispheres (Stone et al., Reference Stone, Flórez-Gonzalez and Katona1990). Félix et al. (Reference Félix, Caballero and Olavarría2007) presents examples of studies conducted in recent years in different locations in the south-eastern Pacific, which have provided an overview of the genetic diversity, which seems to be the lowest among humpback whale stocks in the southern hemisphere, and have shown a migratory relationship between the surveyed feeding areas in the Antarctic and the Colombian and Ecuadorian breeding grounds.

These trans-equatorial migrations between Antarctica and Central America are common for at least part of the humpback whale population in the eastern South Pacific. This area in Central America is considered an overlap area for whales from the northern and the southern hemispheres. Central America is a breeding ground for eastern North Pacific humpback whales migrating from areas off California and also, as reported, a wintering area for whales feeding off Antarctica as well (Félix et al., Reference Félix, Caballero and Olavarría2007). Medrano-González et al. (Reference Medrano-González, Baker, Robles-Saavedra, Murreli, Vásquez-Cuevas, Congdon, Straley, Calambokidis, Urbán-Ramirez, Flórez-González, Olavarría-Barrera, Aguayo-Lobo, Nolasco-Soto, Juárez-Salas and Villavinceio-Llamosas2001) suggests that eastern north and south Pacific populations share genetic traits indicating a trans-equatorial exchange, probably off Central America. When it is the boreal winter season, the austral hemisphere is having its summer season, so that the whales in the southern hemisphere are starting to head south, for their feeding grounds (Rasmussen et al., Reference Rasmussen, Palacios, Calambokidis, Saborío, Rosa, Secchi, Steiger, Allen and Stone2007). Therefore, despite opposite migration schedules, it might be possible for an occasional individual from the southern hemisphere to breed with members of the northern hemisphere population (Stone et al., Reference Stone, Flórez-Gonzalez and Katona1990).

Movements of individuals between feeding and breeding migratory destinations within ocean basins have been extensively demonstrated through the hunting of marked whales, photographic capture–recapture, satellite tagging and telemetry and genetic identification (Mackintosh, Reference Mackintosh1942; Chittleborough, Reference Chittleborough1965). As with trans-oceanic migrations, inter-oceanic migrations appear to be very uncommon among the humpback whales. However, Pomilla & Rosenbaum (Reference Pomilla and Rosembaum2005) reported a match indicating an inter-oceanic migration from an individual from Madagascar and Gabon (Figure 5). The samples belonged to a male individual and shared a locally rare mtDNA lineage. A comparison of dorsal fin characteristics confirmed the genetic match.

Fig. 5. Possible migration routes for humpback whales around Africa. Stars indicate the locations where the two matching samples were collected, in Madagascar and in Gabon. Shading indicates humpback whale distribution in the breeding destinations (white) and in the feeding grounds (dark grey). Dark grey arrows indicate population seasonal migratory routes; white dotted arrows indicate three plausible alternative deviations from the main routes that the sampled individual might have undertaken during a migration from the Indian to the South Atlantic Ocean passing through the feeding grounds (Pomilla & Rosenbaum, Reference Pomilla and Rosembaum2005 and US National Geophysical Data Center; reproduced with permission).

Recent observations of matches (from individual migrators) from different oceans reinforced the idea that humpback whales everywhere are great wanderers both in their regular migrations within the same ocean and in the less frequent trans-oceanic and trans-equatorial migrations (Clapham, Reference Clapham1996).