This study provides unique insights into the niche segregation of two congeneric species throughout their whole annual cycle, by combining at-sea movement, diving, accelerometer, and isotopic datasets. The degree of partitioning was highly stage-dependent, emphasized by the complete niche segregation between CDP and SGDP during the chick-rearing period (Table 3). Such seasonal variation supports the hypothesis that resource partitioning between sympatric similar species increases during energetically demanding periods. The variation between breeding stages was likely related to differences in the processes involved in niche segregation, such as competitive exclusion or niche specialization. In post-breeding, the complete separated migration paths and overwintering grounds of CDP and SGDP may involve processes other than inter-species niche segregation, such as past evolutionary divergence.
Table 3
Summary of spatial (at-sea distribution and dive depth) and trophic segregation between common (CDP) and South-Georgian (SGDP) diving petrels from Kerguelen Islands during the whole annual cycle. The degree of segregation is symbolized as a gradient from no segregation (–) to strong segregation (+++).
| | Degree of segregation | Comment |
Pre-breeding | Distribution | - | Overlapping (both species off-shore) |
Dive depth | | No data |
δ13C (‰) | | No data |
δ15N (‰) | | No data |
Incubation | Distribution | - | Overlapping (both species mostly foraging off-shore) |
Dive depth | - | CDP = SGDP |
δ13C (‰) | + | Large distribution of values for CDP |
δ15N (‰) | + | For similar δ13C, CDP < SGDP |
Chick-rearing | Distribution | +++ | Full spatial segregation (CDP foraging inshore) |
Dive depth | +++ | CDP >> SGDP |
δ13C (‰) | +++ | CDP >> SGDP |
δ15N (‰) | +++ | CDP >> SGDP |
Post-breeding | Distribution | +++ | Full segregation (latitudinal and longitudinal) |
Dive depth | | No data |
δ13C (‰) | ++ | CDP < SGDP |
δ15N (‰) | ++ | CDP > SGDP |
Phenology: influence of oceanographic conditions
In the present study, SGDP started breeding 2-3 weeks earlier than CDP, which was in accordance with historical data from the study site (Weimerskirch et al. 1989). However, this marginal allochrony is inconsistent with the general pattern observed elsewhere in the Southern Ocean (e.g. South-Georgia, Crozet and Kerguelen offshore islands), where CDP typically begin breeding slightly earlier than SGDP (Fig. 1). Timing of breeding is a species/population specific life history trait (Perrins 1970), expected to be synchronized with optimal environmental conditions according to the species ecology. The similar phenology of SGDP populations throughout the species distribution highlights a preference for foraging in offshore waters, where the timing of maximum productivity is constant at a large spatial scale (Labat et al. 2005). Conversely, the substantial variation in the phenology of CDP at both large and local scales (Weimerskirch et al. 1989; Fromant et al. 2020b), may be driven by a stronger influence of local inshore conditions (Weimerskirch et al. 1989).
Interspecific differences in timing of breeding can also be interpreted as a mechanism to reduce competition between ecological similar species (Granroth-Wilding and Phillips 2019). Nevertheless, the relatively long incubation duration of CDP tends to extend the period during which both species share the same foraging area (i.e. during both the incubation and the early chick-rearing periods of SGDP). This, in addition to the important inconsistencies between breeding sites, downplays the importance of such slight allochrony as a competition avoidance induced mechanism.
Incomplete segregation in the early breeding period: competitive exclusion theory
Both CDP and SGDP shared similar pelagic foraging areas during the pre-breeding and incubation periods. For both species, the similarity was emphasized by a clear shift in foraging area from the north-east part of the Kerguelen Plateau in pre-breeding, to the south during the incubation period. Such habitat switching between pre-breeding and incubation is common within seabirds (Cherel et al. 2014; Quillfeldt et al. 2020) and is likely to be related to the limited range that a diving petrel can reach between two incubation shifts (1-3 d; Fromant et al. 2021). As central place foragers, breeding seabirds must find a trade-off between performing short enough foraging trips and accessing productive areas. While the north-eastern sector of the Kerguelen Plateau is highly productive (Blain et al. 2007), its distant location (500-800 km from the study colonies) may force CDP and SGDP to exploit a closer foraging area, matching the requirements of undertaking short incubation shifts.
The exploitation of waters along the south-western shelf-slopes by both species during incubation was characterized by similar trip parameters (trip duration, distance travelled and dive depths). However, and despite large overlap in their isotopic niche, stable isotope analyses revealed subtle trophic differences. For similar values of δ13C (proxy indicating similar water mass), SGDP exhibited slightly higher δ15N values than CDP suggesting that both species may partially differ in their targeted prey. Although both diving petrel species are known to feed on pelagic euphausiid and copepods species (Bocher et al. 2000), the knowledge of their diet during the incubation period is still limited.
During the incubation period, in addition to the difference in blood δ15N values, SGDP exhibited higher diving effort (higher mean VeDBA) than CDP, despite similar dive characteristics (dive depth and duration). The exploitative competition theory (Wootton 1994) predicts that the larger species (CDP) forages more efficiently, thus outcompeting and excluding the smaller one (SGDP). The larger species occupies the niche where intake rates are highest while minimizing diving effort, whereas the smaller species is constrained to increase its diving effort to catch any other available high-quality food. In the scenario where both species target and forage on similar prey patches, the higher effort observed in SGDP imply that they must swim harder to access remaining prey. To supplement their intake under competition, SGDP may need to forage on larger prey that are potentially harder to catch, resulting in the observed higher blood δ15N values and diving effort when compared to CDP. In addition, when the two species fully segregate during the chick-rearing period (see next section), SGDP occupy the niche left vacant by CDP. In particular, this is illustrated by the shift of SGDP isotopic niche towards the niche previously occupied by CDP, supporting the exploitative competition hypothesis.
In South Georgia, the co-existence of CDP and SGDP appears to induce similar exploitative competition during the incubation period, with an isotopic niche segregation arising from SGDP constrained to diving deeper than CDP (Navarro et al. 2014). Similar to Kerguelen, this potential inter-specific competition may result in SGDP pushing the trade-off between prey size and catch towards larger prey (Reid et al. 1997), which would be facilitated by their wider bill compared to CDP (Trallero et al. 2019). However, while body size difference appears to be the main factor driving competitive exclusion, and has been largely documented in various cases in both terrestrial and marine environments (Wearmouth and Sims 2008), our understanding of such predator-prey interactions will remain unclear without direct observation of foraging behaviour in the field.
Complete niche segregation in chick-rearing: niche specialization theory
During the chick-rearing period, CDP and SGDP fully differed in their at-sea distribution, diving behavior and isotopic niche. This substantial change in the degree of segregation between the two species was driven by a drastic shift in CDP foraging ecology. While SGDP foraged in similar offshore areas and depths during both the incubation and chick-rearing periods, CDP foraging habitat during chick-rearing was restricted to the coastal area (Golfe du Morbihan), switching from open ocean to a semi-closed embayment. This resulted in a substantial decrease in trip duration and distance travelled than during incubation, and when compared to both the incubation and chick-rearing periods of SGDP. This profound shift in at-sea distribution of CDP during the chick-rearing period coincided with substantial modifications in their diving behaviour (increased depth, duration and mean VeDBA per dive).
The change in foraging niche occupied by CDP during the incubation and chick-rearing periods is further supported by the substantial shift in isotopic niche. This complete spatial and isotopic niche segregation has been previously illustrated by stomach content analyses, showing that CDP rely mostly on the swarming amphipod Themisto gaudichaudii during this period (Bocher et al. 2000). In the Golfe du Morbihan, this crustacean displays a strong seasonal variation with a peak of abundance in summer (Labat et al. 2005), precisely matching the chick-rearing period of CDP. As income breeders (Chastel et al. 1995), diving petrels are expected to match the energy-demanding chick-rearing period with a peak of resource availability (Perrins 1970). Thus, it is likely that the observed switch in CDP foraging habitat between incubation and chick-rearing is triggered by the summer high density of T. gaudichaudii in the Golfe du Morbihan (Bocher et al. 2001).
In addition, the overall pattern of isotopic values shifting from offshore to inshore environments between incubation and chick-rearing masks the fact that some CDP individuals already started feeding in the Golfe du Morbihan while still incubating. This suggests that CDP switched foraging behaviour as soon as T. gaudichaudii became available within the gulf. Such results may provide key information to understand the process of niche segregation between CDP and SGDP. Indeed, surprisingly, SGDP did not appear to take advantage of this reliable and locally superabundant prey during neither the incubation period nor the energetically demanding chick-rearing period.
Spatial and trophic segregations are considered to result from competitive exclusion (the bigger species accessing the best resource), or niche specialization (induced by morphological and/or physiological differences) (Phillips et al. 2004). Although, both processes may be applicable in the present case, the total absence of SGDP from the T. gaudichaudii niche strongly suggests partitioning arising from physical capabilities and diving performance. Indeed, for a breath-hold diving species, maximum dive depth and duration generally increase with body mass (Schreer and Kovacs 1997), while prey capture is proportional to the time that an individual allocates to the bottom phase of a dive (Wilson 2010). Following the model of depth/time relative efficiency developed by Wilson (2010), CDP appears to be the most efficient of the two species at depths in excess of 10 m.
The relative absence of surface feeders in the Golfe du Morbihan (Bocher et al. 2001; Cherel et al. 2014), in addition to the depths exploited by CDP and coastal penguin species feeding on T. gaudichaudii (Bocher et al. 2000, 2001), confirm that this abundant prey is mainly restricted to depths deeper than 10 m. Therefore, the relatively lower efficiency of SGDP at deeper depths, associated with their smaller body size, may restrict their access to T. gaudichaudii in the Golfe du Morbihan. Although SGDP are able to dive as deep as 20 m, when compared to CDP for similar dive depth and duration, the higher mean VeDBA observed for SGDP suggests these individuals have a lower diving capacity.
In addition, the lower wing loading of SGDP may also reflect their adaptation to flying over longer distances than CDP (Thaxter et al. 2010). Notable differences in diving performances and energetic expenditure of the SGDP appear to be key factors explaining the use of distant areas to target more accessible prey species at shallower depth. For SGDP, the energetic cost of repeated deep and long dives may exceed the cost of undertaking longer trips but foraging on more accessible prey in conditions of limited exploitative competition. Therefore, the complete niche segregation observed between CDP and SGDP during the chick-rearing period may result from niche specialization and not direct competition.
At South Georgia, Reid et al. (1997) reached the same conclusions based on stomach content analyses of both species during the chick-rearing period, interpreting the difference in targeted prey as differential diving capabilities. In the extensive literature exploring niche partitioning between similar species or sex, niche specialization commonly originates from body size differences and divergent relative efficiencies to exploit the environment (Wearmouth and Sims 2008). For example, the between-sex difference in wing loading for albatrosses may advantage females in lower wind conditions (Phillips et al. 2011), which ultimately appears to induce latitudinal habitat specialization (Weimerskirch et al. 1997; Phillips et al. 2004). Similarly, niche segregation in alcids during the chick-rearing period appears to be caused by differential flying and/or diving capabilities (Thaxter et al. 2010).
Post-breeding migration: historical distribution and congeneric segregation
During the inter-breeding period, CDP and SGDP headed in divergent directions and different latitudes. The stable isotopic signatures in body feathers supported the idea of latitudinal segregation, with lower δ13C values for CDP indicating a moulting area farther south than for SGDP (Jaeger et al. 2010). Adult diving petrels migrate to wintering areas directly after the end of the breeding season (Rayner et al. 2017; Fromant et al. 2020b), and renew their plumage during the first months of this period (Fromant et al. 2020b). Because moult is an energetically/nutritional demanding process, seabirds are likely to renew their plumage where the surrounding waters are productive (Cherel et al. 2016), which may incite ecologically similar species to migrate to different areas. Previous studies on winter distribution of small petrels and prions showed clear inter-species latitudinal segregation, which was explained by differences in preferred water masses (Quillfeldt et al. 2015).
Interestingly, the recent studies investigating the post-breeding distribution of three different diving petrel species (Navarro et al. 2015; Rayner et al. 2017; Fromant et al. 2020b; Fischer et al. 2021; present study) all revealed that diving petrels migrate to well defined population/species-specific areas. This contrasts with the highly dispersive behavior generally observed with other small-sized procellariiform species (Quillfeldt et al. 2015; Navarro et al. 2015). In particular, the ecological theory of segregation predicts that individuals should disperse when they are no longer tied to their breeding grounds. Therefore, the observed segregation in migration area may not be a response to the selective pressure arising from present competition avoidance between sympatric species, but instead, could reflect past evolutionary divergence (Peck-Richardson et al. 2018). Divergent but consistent species-based and population-based cultural patterns may suggest that each species/population is responding to different life history traits. The evolution of wintering ecological optimum for each species/population may, therefore, involve historical distribution shift of water masses but also the sequence of colonization(s) and speciation within diving petrels.
In addition, by heading south-east, Kerguelen SGDP may as well segregate from large populations of conspecifics breeding on Crozet Islands. Two species can indeed segregate in other dimensions than space when their distribution overlaps, while two synchronous populations of the same species must segregate spatially in order to avoid competition for the same resource. Thus, perceived inter-breeding segregation between sympatric sibling species could rather result from intra-species (populations) competition avoidance.