ICES Journal of
Marine Science
ICES Journal of Marine Science (2014), 71(9), 2589– 2598. doi:10.1093/icesjms/fsu093
Original Article
Biomass consumption by breeding seabirds in the western Indian
Ocean: indirect interactions with fisheries and implications for
management
D. K. Danckwerts1*, C. D. McQuaid 1, A. Jaeger2, G. K. McGregor 3, R. Dwight 3, M. Le Corre2,
and S. Jaquemet 2,4
1
Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa
Laboratoire ECOMAR (FR3560 UR/CNRS-INEE), Université de La Réunion, 15 Avenue René Cassin, CS 92003, 97744 St Denis Cedex 9, Ile de La Réunion,
France
3
Department of Geography, Rhodes University, Grahamstown 6140, South Africa
4
UMR EME 212 (IRD/IFREMER/UM2), Department of Botany, Rhodes University, Grahamstown 6140, South Africa
2
*Corresponding author: tel: +27 46 603 8525; fax: +27 46 622 8959; e-mail: [email protected]
Danckwerts, D. K., McQuaid, C. D., Jaeger, A., McGregor, G. K., Dwight, R., Le Corre, M., and Jaquemet, S. Biomass consumption by
breeding seabirds in the western Indian Ocean: indirect interactions with fisheries and implications for management. – ICES
Journal of Marine Science, 71: 2589 – 2598.
Received 7 October 2013; revised 14 April 2014; accepted 27 April 2014; advance access publication 6 June 2014.
Fisheries potentially affect seabirds both directly and indirectly. Well-documented direct effects have resulted in significant losses to seabird populations, but indirect effects are less well known. One way in which tropical seabirds may be indirectly affected is through overexploitation of
large subsurface predators. Tropical seabirds must forage over wide areas to attain sufficient prey and have evolved various methods of increasing
foraging efficiency. One strategy is their association with surface-feeding tunas. When feeding, these predators drive prey to the surface, making them
available to seabirds feeding from above. Losses in predator biomass will reduce prey accessibility (but not necessarily prey abundance) for seabirds,
contributing to declines in bird populations. To explore indirect fisheries effects, we compared estimates of the magnitude and spatial distributions
of consumption by breeding seabirds with fisheries offtake in the western Indian Ocean (WIO). Data from the literature were compared with Indian
Ocean Tuna Commission longline and purse seine landings of selected tuna and billfish species from between 2000 and 2009. Breeding seabird
populations (adults and immature birds) were estimated at 19 million individuals, assuming 50% breeding success. Based on the literature,
these birds will consume between 150 000 and 500 000 metric tonnes (t) of prey; values that are of the same magnitude as mean annual longline
(904+632 t) and purse seine (349 861+61 820 t) landings for the region. Spatial overlap between fisheries and seabirds is high, especially around
the Seychelles, suggesting that the indirect impacts of fisheries on seabird populations may be great. Sooty Tern (Onychoprion fuscatus) is by far
the dominant seabird in the study area, accounting for over 80% of numbers and consumption estimates. Our results highlight the importance
of seabirds within WIO marine trophic webs and emphasize the potential indirect effects of industrial tuna fisheries on their populations.
Keywords: longline, prey accessibility, purse-seine, sooty tern, subsurface predators, tropical seabird, tuna.
Introduction
The importance of seabirds within marine ecosystems is becoming
increasingly recognized (Schreiber and Burger, 2002). Indeed,
recent research has shown that the annual biomass consumed by
seabirds is equivalent to the tonnage of marine resources removed
each year by industrial fishing practices (Brooke, 2004). But while
seabirds are gaining scientific appreciation, the future of their populations remains uncertain. The human population, characterized by
# International
an unparalleled growth, has now exceeded 6.1 billion individuals
and has been shown to be directly correlated with species extinctions
(Soulé, 1991; Steadman, 1995). One-fourth of all bird species are
believed to have gone extinct as a result of human activities and
seabird groups, most notably the Procellariiformes, are among the
most threatened of all (Soulé, 1991; Steadman, 1995; Dee
Boersma et al., 2002). This is especially true for the biodiverse
western Indian Ocean (WIO) where a decline in seabird populations
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2590
has been observed since the 18th century (Feare, 1978, 1984). Many
colonies are now extinct and those that still exist are greatly reduced
in size (Feare, 1984; Feare et al., 2007). Some of the greatest threats
facing seabirds today relate to industrial fishing practices (Tasker
et al., 2000), and while a considerable degree of scientific attention
has been devoted to understanding the direct effects of fishing activities on seabird populations, very little is known about the potential
indirect impacts of these activities on the birds (reviewed in
Montevecchi, 2002).
One way in which tropical seabirds might be indirectly affected
by fishing practices is through the overexploitation of large subsurface predators (Le Corre and Jaquemet, 2005). Unlike temperate and
polar species, few tropical seabirds are able to access the water
column through diving and most must search wide areas to
obtain sufficient prey (Ballance and Pitman, 1999). To increase foraging efficiency, these birds have evolved an association with feeding
subsurface predators, mainly schooling tuna and dolphins. The predators, when feeding, drive forage fish to the surface making them
available to seabirds feeding from above (Au and Pitman, 1986;
Ballance and Pitman, 1999; Le Corre and Jaquemet, 2005). Some
seabird species are even regarded as “near obligate commensals”
of tuna with more than 70% of all feeding activity occurring in association with schools of large predatory fish (Au and Pitman, 1986;
Harrison and Seki, 1987; Jaquemet et al., 2004). As such, declines
in tuna populations are thought to affect seabird populations by indirectly decreasing the prey available to them (Au and Pitman, 1986;
Harrison and Seki, 1987; Le Corre et al., 2012).
Until very recently, fisheries management has attempted to increase target fish catches, while ignoring the unintended ecosystem
consequences. But the overall risks associated with seabird–fishery
interactions have led to various international conservation agreements including the International Plan of Action (IPOA) for
Reducing Incidental Catch of Seabirds in Longline Fisheries [under
the United Nations Food and Agriculture Organization (FAO)], the
United Nations Convention on the Law of the Sea, and the
Agreement on the Conservation of Albatrosses and Petrels. These
agreements address the critical need for a more effective and holistic
approach to fisheries management, by promoting ecosystem-based
management (EBM; Yodzis, 2001; Pikitch et al., 2004). EBM places
considerable emphasis on the sustainable use of marine resources,
while also attempting to reduce the non-target species and habitat
impacts of human activities (Pikitch et al., 2004). Particular emphasis
is given to fisheries considering the influence that these practices
have on fish abundance, trophic structure, ecosystem integrity,
and marine biodiversity (Pikitch et al., 2004). In fact, EBM is
also referred to as ecosystem-based fisheries management (EBFM)
and ecosystem-approach to fishery management (EAFM; Pikitch
et al., 2004).
EBM management will remain controversial until the numerical
relationships between predators and prey are quantified and such
an approach implies the need to estimate the flux of biomass that
exists through marine ecosystems (Pikitch et al., 2004; Cury et al.,
2011). Therefore, as an initial step towards EBFM, we conducted
the first estimation of biomass consumption by breeding seabirds
in the WIO, a region where tuna fisheries are well developed and
tuna constitute the main overall catches. These biomass intakes
were compared with Indian Ocean Tuna Commission (IOTC)
longline and purse-seine landings of selected tuna and billfish
species for the period 2000 – 2009. Our intention was to identify
the areas where the impacts of intensive fisheries on seabird populations are likely to be greatest, by examining bird consumption,
D. K. Danckwerts et al.
during the breeding season, and fishery catches on a spatially
explicit basis.
Study area and methods
For the purposes of this study, the WIO is defined as the area
between 508E and 758E, and 308S and 208N. Seabird colonies were
lumped into five groups roughly corresponding to the five main
regions of the WIO, namely the Mascarenes, the Seychelles, the northern, and southern Mozambique Channel, and the Somalia and
Red Sea regions (Figure 1).
All 30 breeding seabird species from the 54 known colonies
(Figure 1) in the region were included in our calculations. Many
transient and vagrant species are found within the study area, but
these were excluded because of the difficulty of estimating their
abundance and because there is a great deal of the uncertainty
regarding their diet when they are present in the region.
Calculation of the biomass consumed by seabirds
The range of biomass consumed by each species was calculated as the
product of a population estimate (number of individuals), the daily
biomass consumed (t d21), and a period of time (days). Seabird
populations were estimated using an existing database of breeding
population size of different species at different colonies across the
WIO (data from Baker and Baker, 2001; Bennun and Njorge,
2001; Le Corre and Safford, 2001; Robertson, 2001; Rocamora and
Skerrett, 2001; Safford, 2001a, b; Le Corre and Jaquemet, 2005;
Feare et al., 2007). It was assumed that a single chick is produced
by every breeding adult pair (Weimerskirch, 2002), corrected with
50% breeding success. Although Brooke (2004) estimated seabird
populations using 60% survival, Catry et al. (2013) showed considerable interannual variation in the breeding performance of four
tern species at Aride Island in the Seychelles. This ranged from complete failure in some species in some years to 91.5% fledgling success
in other species in other years. The average breeding success of the
four species studied over 4 years only marginally exceeded 50%
and so this value was deemed most appropriate in our study. In addition, data owned by MLC and SJ and their experience on most of the
tropical seabird species in the region support the suggestion of 50%
breeding success. The units of time used in these calculations were
the number of days within a single calendar year that each species
is associated with the breeding colonies, taken from Appendix 2 in
Schreiber and Burger (2002). We refer to this time, which extends
from the pre-laying period through to the end of the post fledging
dependence (where applicable), as the breeding season. This
ranged from a minimum of 40 days in smaller species, such as the
Saunder’s Tern (Sterna saundersi), to a full year for larger species like
the Great Frigatebird (Fregata minor), which show extended parental
care. In this regard, we also use the term “immature” to encompass the
various growth stages that young birds must go through before they are
completely independent of their parents. No distinction was made
between the active breeding season when energy constraints on the
adult birds are higher and otherwise. Rather, consumption was calculated using the known range of daily biomass consumption and the
length of breeding season, providing conservative and liberal estimates
of the tonnage removed. During the breeding season, adults are constrained by the energy demands of their offspring and remain within
the vicinity of the colony, though some species do forage over great distances (up to 1000 km) at this time (Weimerskirch et al., 2004; Pinet
et al., 2011). There is considerable evidence to suggest that many
species disperse widely when at sea during the interbreeding period
with some also undertaking long distance migrations within [e.g.
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Biomass consumption by breeding seabirds
Figure 1. The WIO is a biodiverse region hosting globally significant populations of seabirds. Fifty-four extant breeding colonies are known to exist
and are as follows: (1) Jasiira Ceebaad and Jasiira Sacada Din, (2) Jasiira Maydh, (3) Socotra Group, (4) Raas Xaafun and Raas Gumbax, (5) Mogadisho
Islets, (6) Bajan islands, (7) Kiunga Marine Nature Reserve, (8) Whale Island, (9) Kisite Island, (10) Zanzibar Chumbe Island, (11) Latham, (12) Mafia
Island, (13) Aride, (14) Bird Island, (15) Cousin, (16) Cousine, (17) Frégate, (18) Récif, (19) African Banks, (20) Boudeuse, (21) D’Arros, (22) Desnoeufs,
(23) Marie-Louise, (24) Farquhar, (25) Goelettes, (26) Aldabra, (27) Cosmoledo, (28) Glorieuses, (29) Mayotte, (30) Mohéli, (31) Cape Anorontany
Archipelago, (32) East Coast of Ansiranana, (33) Mitsio Archipelago, (34) Nosy Bé and other islets, (35) Etoile, (36) Puga-Puga, (37) Juan de Nova, (38)
Nosy Barren, (39) Europa, (40) Islets off Morombé, (41) Nosy Vé, (42) Nosy Manitra and other islets, (43) Ilôts off Toamasina, (44) Tromelin, (45)
Réunion, (46) Flat Island, (47) Gabriel Island, (48) Gunner’s Quoin, (49) Pigeon Rock, (50) Round Island, (51) Serpent Island, (52) Saint-Brandon, (53)
Rodrigues Islets, and (54) Chagos Archipelago.
Brown Noddy (Anous stolidus)] and outside the WIO [e.g. Sooty Tern
(Onychoprion fuscatus) and Barau’s Petrel (Pterodroma baraui); pers.
unpub. data; Pinet et al., 2011; Le Corre et al., 2012]. Consequently,
consumption was calculated only for the breeding population
(adults and immature birds) during the breeding season. Finally, the
relative contribution of fish, fish larvae, crustaceans, and cephalopods
to the diets of adults and immature birds of each species were extracted
from the literature. Information on stomach content weights and the
number of meals received each day were used to calculate the daily
biomass consumption of immature birds, whereas the consumption
of adults was calculated using field metabolic rates (FMRs) and prey
energy contents assuming 75% digestive efficiency (Jackson, 1986;
Hilton et al., 1999; Brooke, 2004). Prey proportions of closely
related species were used when the required data were unavailable
and FMRs were calculated using mass-based equations (Nagy, 1987;
Birt-Friesen et al., 1989; Nagy et al., 1999; Ellis and Gabrielsen,
2002). Energetic values for each of the four prey groups were extracted
from Davis et al. (1998) and Harris et al. (1986) as follows: crustaceans
2 kJ g21, cephalopods 5.5 kJ g21, fish 5.7 kJ g21, and fish larvae
4.98 kJ g21. More detailed descriptions of the calculations, including
examples, are provided in Supplementary material.
The four different prey groups were not individually analysed
and no distinction was made between adults and immature birds.
Rather, the data were analysed, by species, colony, and region. The
six dominant species (in terms of consumption) within each main
region of the WIO were selected for more detailed analyses of population size and estimated consumption. Together, these species
account for over 95% of the overall seabird populations (by
number) and 97% of the overall biomass consumption (see the
Results section). The remaining species within each region were
lumped into a seventh category labelled “Other”. Results were tabulated and analysed using Microsoft Office 2007 packages and
mapped using ArcGIS10.
Analysis and comparison with industrial fisheries landings
The estimates of seabird consumption were compared with the
mean annual IOTC purse-seine and longline landings of selected
tuna and billfish species for the period 2000–2009. These data can
be downloaded directly from the IOTC databases (www.iotc.org/
English/data.php). Fisheries data were analysed using R.3.0.1. and
were spatially mapped using ArcGIS10 packages.
Results
Seabird population sizes
The breeding seabird population of the WIO was estimated at 19
million individuals. The Sooty Tern accounts for 85% of this estimate, while the Lesser Noddy (A. tenuirostris), Wedge-tailed
Shearwater (Puffinus pacificus), and Brown Noddy together contribute an additional 11% to the total population. The remaining
2592
26 species, together, account for only 4% of the overall seabird
population within the region.
The Sooty Tern was the most abundant species in the Mascarenes
(64%), Seychelles (79%), northern (99%), and southern (98%)
Mozambique Channel regions, but was replaced by the Socotra
Cormorant (Phalacrocorax nigrogularis) around Somalia and the
Red Sea. In this last region, the Socotra Cormorant accounts for
22% of the local seabird population, while the Sooty Tern constitutes only 0.2% of the birds there (Table 1).
Seabird populations are centred on the Seychelles Archipelago
(Figure 2a). Twenty-three of the 54 known colonies are found
there, supporting 51% of all breeding seabirds in the WIO
(Figures 1 and 2a). Some of the largest colonies are found within
this area, including Cosmoledo (+2 900 000 birds), Bird Island
(+1 800 000 birds), Aride Island (+1 400 000 birds), and Chagos
(+1 000 000 birds; Figure 2a). The largest breeding colony is,
however, Juan de Nova (+5 000 000 birds) in the northern
Mozambique Channel (Figure 2a). This region hosts 30% of the
breeding birds in the WIO, while the Mascarenes and southern
Mozambique Channel together host a comparatively small 19% of
seabirds. The lowest population was recorded from around
Somalia and the Red Sea, comprising only 1% of the total estimate
(Table 1).
Biomass consumed by seabirds
Based on the population sizes, the biomass consumed by breeding seabirds was calculated as between 150 000 and 500 000 t
(Table 1). The relative contribution of each species to the total consumption differed slightly from the patterns observed in population
sizes. The Sooty Tern was once again the dominant species overall,
accounting for 81% of consumption, while the Lesser Noddy,
Wedge-tailed Shearwater, Red-footed Booby (Sula sula), and
Masked Booby (S. dactylatra) together added an additional 12%.
The remaining 25 species accounted for only 7% of the estimated
consumption.
At a regional scale, the importance of each species to the consumption was variable, but the Sooty Tern was again dominant
across all regions except around Somalia and the Red Sea where it
was replaced by the Brown Booby (Sula leucogaster) and Socotra
Cormorant (Table 1). This region is unusual in that it is dominated
(in both consumption and population) by a number of species,
which are endemic, or nearly endemic to the region.
The spatial distribution of consumption mirrored the heterogeneous distribution of seabird populations during the breeding
season (Figure 2b). The highest overall consumption was recorded
for Juan de Nova (26%), with significant contributions also
recorded from Cosmoledo (16%), Europa (10%), Bird Island
(10%), Aride (7%), and Chagos (6%; Figure 2b). The remaining
49 colonies accounted for 25% of the total estimated consumption.
At a regional scale, the Seychelles accounted for 51% of consumption and the northern Mozambique Channel contributed an
additional 29% (Table 1). The southern Mozambique Channel
and Mascarene regions together accounted for 18% of the consumption estimates, while Somalia and the Red Sea contributed the final
2% (Table 1).
Longline and purse-seine catches
Purse-seine fishing dominates the catches in the WIO, removing 349
861 + 61 820 t annually over the period 2000–2009. Longline
fishing removes significantly less, with 904 + 632 t of tuna and billfish caught annually over the same period.
D. K. Danckwerts et al.
Purse-seine and longline landings were heterogeneously distributed in both space and time. Overall landings are moderately higher
during summer when longline and purse-seine fishing removed
52.3 and 55.4% of the total landings, respectively (Figure 2c
and e). At this time, the main longline tonnage was removed from
the area between 258S and 408S and immediately around the
Seychelles and the Mascarene islands (Figure 2c). In contrast, purseseine landings were concentrated between the Seychelles and East
Africa, extending northwards towards Somalia and Oman, and eastwards towards the Chagos Archipelago (Figure 2e). Landings during
winter, 47.7% for longline and 44.6% for purse-seine, were only
marginally lower (Figure 2d and f). Longline landings were more
concentrated within the same regions (Figure 2d), accompanied
by a southeastward contraction in purse-seine landings (Figure 2e).
Discussion
Our results provide an estimate of total prey offtake by breeding seabirds in the WIO of between 150 000 and 500 000 t, consumed by
nearly 19 million individuals. Importantly, using a conservative approach, this estimate is of the same order of magnitude as the annual
landings of tuna and billfish in the region. This highlights the importance of seabirds as a component of the marine ecosystem in the WIO,
as they consume a significant proportion of the production by the
lower trophic levels. There have been similar findings for other
oceanic regions (e.g. Harrison and Seki, 1987; Guinet et al., 1996;
Barrett et al., 2002) and even at a global scale (Brooke, 2004). This
does not necessarily imply that seabirds and fisheries are in competition, but it does imply important ecosystem consequences that are
largely unknown at this stage (Brooke, 2004; Cury et al., 2011).
Seabird populations and biomass consumption in the WIO
Because of its numerical dominance, the spatial distribution of the
total seabird populations in the WIO mirrors that of the Sooty Tern
and the highest concentrations of birds were found where this
species is the most abundant. Sooty Terns accounted for over 85%
of all seabirds in the study area and were especially abundant
around the northern Mozambique Channel and the Seychelles.
Significant breeding colonies are also known from the southern
Mozambique Channel and the Mascarenes, while gatherings of
unknown sizes are found in the Maldives (Feare et al., 2007).
Interestingly, moderately high seabird biomass was also recorded
in the areas surrounding Somalia and the Red Sea where the Sooty
Tern occurs in very low abundance and biomass is instead dominated
by a suite of species not found elsewhere in the WIO. These include the
Socotra Cormorant, Red-billed Tropicbird (Phaethon aethereus),
White-eyed Gull (Ichthyaetus leucophthalmus), Persian Shearwater
(Puffinus persicus), and Jouanin’s Petrel (Bulweria fallax).
There is a very close relationship between the population size of a
species and our estimate of its consumption. Not surprisingly then,
the highest estimates of consumption by seabirds were recorded
from the northern Mozambique Channel and the Seychelles, corresponding to those areas where Sooty Tern is most numerous.
Nevertheless, on an individual basis, larger species tend to
consume more that smaller ones, explaining the slight discrepancy
between the numerically dominant species and those which
account for the most consumption.
The Sooty Tern was ranked as fourth in terms of annual biomass
consumption on a global scale by Brooke (2004), being the only
tropical species comparable with many high latitude birds, and
dominated consumption in our study. Indeed, the Sooty Tern is
widely accepted as the most abundant tropical seabird worldwide
2593
Biomass consumption by breeding seabirds
Table 1. Regional breeding population size (adults and immature birds) and estimated biomass consumption (t year21) by dominant seabird
species in the WIO.
Consumption by
breeding birds
(adults and chicks)
Region
Mascarenes
Common name
Sooty Tern
Wedge-tailed Shearwater
Lesser Noddy
Brown Noddy
Masked Booby
Red-tailed Tropicbird
Other
Seychelles
Sooty Tern
Lesser Noddy
Red-footed Booby
Wedge-tailed Shearwater
Masked Booby
Brown Noddy
Other
Southern Mozambique
Sooty Tern
Red-footed Booby
Lesser Frigatebird
Red-tailed Tropicbird
Greater Frigatebird
Roseate Tern
Other
Somalia and Red Sea
Brown Booby
Socotra Cormornat
Brown Noddy
Persian Shearwater
White-eyed Gull
Masked Booby
Other
Northern Mozambique
Sooty Tern
Greater Crested Tern
Brown Booby
Masked Booby
Lesser Frigatebird
Caspian Tern
Other
Scientific name
Onychoprion fuscatus
Puffinus pacificus
Anous tenuirostris
Anous stolidus
Sula dactylatra
Phaethon rubricauda
N/A
Regional totals
Onychoprion fuscatus
Anous tenuirostris
Sula sula
Puffinus pacificus
Sula dactylatra
Anous stolidus
N/A
Regional totals
Onychoprion fuscatus
Sula sula
Fregata ariel
Phaethon rubricauda
Fregata minor
Sterna dougallii
N/A
Regional totals
Sula leucogaster
Phalacrocorax nigrogularis
Anous stolidus
Puffinus persicus
Ichthyaetus leucophthalmus
Sula dactylatra
N/A
Regional total
Onychoprion fuscatus
Thalasseus bergii
Sula leucogaster
Sula dactylatra
Fregata ariel
Hydroprogne caspia
N/A
Regional total
Grand total
and the biodiverse WIO is known to host globally significant populations of this species (Schreiber et al., 2002; Feare et al., 2007).
During the breeding season, these birds nest in large, synchronized,
and extremely dense colonies that frequently exceed 100 000 pairs
(Le Corre and Jaquemet, 2005; Feare et al., 2007) and Juan de
Nova in the northern Mozambique Channel is one of the largest
tropical seabird colonies in the world, hosting some 2 million breeding Sooty Tern pairs (Feare et al., 2007).
Globally, the distribution of seabird colonies and seabird abundances have been related to the availability of suitable nesting areas
(Bailey, 1968) and to the accessibility and predictability of food
during the breeding season (Lack, 1968; Jaquemet et al., 2007).
The WIO in particular is a hotspot of marine and terrestrial biodiversity (Myers et al., 2000), and this is partly a consequence of
the geomorphology of the region. Several islands of different ages,
Breeding population
88 1125
229 075
127 500
92 250
1 275
6 575
46 231
1 384 031
7 657 625
1 060 000
84 525
246 075
31 113
257 750
338 383
9 675 471
1 900 250
7 500
6 000
9 613
2 750
13 700
3 463
1 943 276
37 750
38 000
50 000
25 000
2 500
500
17 000
170 750
5 710 000
27 725
775
200
250
125
3163
5 742 238
18 915 766
Min (t)
5 725
4 950
662
607
104
106
470
12 624
49 343
5 507
6 921
5 318
2 532
1 695
4 398
75 712
12 362
618
360
155
235
37
39
13 806
2 248
1 454
329
180
48
41
97
4397
38 185
386
46
16
15
4
27
38 680
145 220
Max (t)
21 745
8 745
2 221
1 802
381
324
1 038
36 257
187 660
18 468
12 071
9 394
9 282
5 036
10 266
252 176
47 961
1 078
627
474
446
124
77
50 787
6 772
2 617
977
394
372
149
261
11 542
144 807
1 260
139
60
26
24
64
146 380
497 142
sizes, and origins are spread throughout the region hosting a very
high diversity and abundance of species, including seabirds. At the
basin scale, the western part is the most productive region of the
Indian Ocean because of the many seasonal upwelling cells that
develop (Bakun et al., 1998) and the strong mesoscale oceanographic activity in the Mozambique Channel (Tew Kai and Marsac, 2010).
More specifically, environmental predictability is associated with
large, persistent hydrological structures such as the Indian Ocean
South Equatorial Current (SEC), the succession of mesoscale
eddies in the Mozambique Channel (Zubkov and Quartly, 2003),
and the seasonal upwelling off Somalia, which develops during
the southwest Indian monsoon season (Schott et al., 2002).
Associated with these features are a high diversity and biomass of
marine organisms (Bakun et al., 1998), including zooplankton
and micronekton (Sabarros et al., 2009), flying fish (Plomley, 1968;
2594
D. K. Danckwerts et al.
Figure 2. Population size (a) and estimated biomass consumption (b) of seabirds at colonies in the WIO, as is compared with the spatial
distribution of mean (2000 – 2009) longline and purse-seine landings during summer (c and e) and winter (d and f), respectively.
Piontkovski and Williams, 1995), and also the tunas (Fonteneau,
1997; Worm et al., 2005; Tew Kai and Marsac, 2010) and the
marine mammals that increase prey accessibility for tropical seabirds.
Consequently, the western part is also the most productive region of
the Indian Ocean in terms of industrial fisheries landings and the area
where the diversity of catches is greatest (Fonteneau, 1997).
Sources of error and comparison with other oceanic
regions
This is only the second attempt at estimating seabird consumption
over a tropical region (see Harrison and Seki, 1987), and this assessment for the WIO provides a first order of magnitude of biomass
uptake by tropical seabirds. Several potential errors complicate
Biomass consumption by breeding seabirds
the estimation of total food consumption however. These arise from
uncertainties concerning the diet of several species, including
almost all species from the Somalia and the Red Sea region, and
the sizes of breeding populations in several areas (e.g. Sooty Terns
in the Maldives). In addition, almost all data relating to nonbreeding and pre-breeding birds are lacking. Various authors (e.g.
Harrison and Seki, 1987; Cairns et al., 1991; Brooke, 2004) have provided means by which to calculate their populations, but they
assume that all birds return to the region when the breeding population does so. An unknown proportion will almost certainly do so,
but tracking data suggest that at least some will remain in more productive waters elsewhere (unpub. data, MLC, SJ). Similarly, the proportion of birds that remain within the WIO during the
interbreeding period when others migrate elsewhere is not known,
and recent evidence suggests that these movements vary considerably between species and colonies (unpub. data, MLC, SJ). This,
combined with the uncertainties on their dietary habits, would
only act to confound our results and hence their exclusion from
this first estimation. These points also hold true for vagrants and
large seasonally visiting species, such as albatrosses (Cherel et al.,
2013), that can remove significant quantities of marine resources
each year. For these reasons, our work serves as a conservative first
estimation that nevertheless indicates the magnitude of seabird consumption in the region.
We also note that that our estimation of biomass uptake by seabirds is smaller than those for higher-latitude ecosystems, which
have an equivalent or fewer number of birds (e.g. Woelher and
Green, 1992; Guinet et al., 1996; Barrett et al., 2002). This simply
reflects the average body mass of the species involved and the associated energy requirements, which are smaller in tropical species.
A calculation for the seabirds of the Hawaiian Archipelago constitutes the only other estimation for a tropical ecosystem and produced
results of a similar order of magnitude to ours despite bird numbers
being less than one-third that of the WIO, even after the inclusion of
non-breeding groups (Harrison and Seki, 1987). This reflects the
dominance of large (.2.5 kg) tropical albatrosses around Hawaii
and their higher energy requirements and daily consumption.
Importantly, consumption from the Hawaiian study will have
been gathered from a much greater area than within our study
region. Breeding Laysan Albatrosses (Phoebastria immutabilis) will
often travel up to 10 000 km from Bird Island in the Hawaiian
Archipelago during a single foraging trip (Kappes et al., 2010).
Combining the inclusion of non-breeding and visiting birds with
the spatial concentration of seabird consumption in the WIO
emphasizes their importance in these foodwebs. Critically, as for
the Sooty Tern, Wedge-tailed Shearwater, and Red-footed Booby
in our study, the second most important feeding guild in the
Hawaiian ecosystem comprised seabirds which feed in association
with surface predatory fish (Harrison and Seki, 1987).
Seabird consumption compared with fisheries activities
The WIO is one of the world’s most productive regions in terms of
the annual tuna and billfish landings (Fonteneau, 1997; Worm et al.,
2005; Juan-Jordá et al., 2011). Consequently, our principal results
are that the substantial consumption of marine resources by breeding seabirds in the WIO is comparable with the combined longline
and purse-seine landings for the region and, not unexpectedly, that
there is considerable spatial overlap between the two groups. The
first finding is similar to those from other comparisons between
seabird consumption and fisheries landings (e.g. Brooke, 2004;
Karpouzi et al., 2007). Importantly, however, fisheries catches for
2595
the WIO do not include illegal, unregulated, and unreported
(IUU) offtake. Incorporating IUU estimates into our calculations
(Agnew et al., 2009), longline and purse-seine landings rise to
1000 and 420 000 t, respectively, but are still directly comparable
with our estimates of bird offtake during the breeding season. Given
the conservative nature of our estimates, this emphasizes the importance of seabirds within the marine foodwebs of the WIO but
does not necessarily imply direct competition between seabirds
and fisheries. On the contrary, competition is only expected in
instances where both groups target the same prey species/groups
in the same areas (Brooke, 2004).
Assuming phytoplankton occupy a trophic level (TL) of 1, food
fish theoretically then occupy TLs of between 3 and 4.5, ranging
from small forage fish to large tropical tunas and billfish (Pauly
et al., 2002). Humans have preferentially targeted the higher
trophic level species (Collette et al., 2011), and a decline of 0.05 –
0.10 TLs per decade has been observed in global fish stocks, suggesting that humans are “fishing down foodwebs” (Pauly et al., 1998).
Indeed, recent research has shown that 63.3% of the adult tuna
biomass was lost from the WIO between 1954 and 2006, constituting
the greatest loss at the global scale exceeding both the Pacific
(249.2%) and Atlantic Oceans (249.6%; Juan-Jordá et al.,
2011). While this implies major changes to marine foodwebs, it
does not necessarily imply that the forage fish stocks are declining
in the region. The mesopredator release hypothesis suggests that
top-down forces (e.g. predation) limit the populations of these
groups and if released, their populations can be expected to increase
(Frank et al., 2005; Baum and Worm, 2009; Ferretti et al., 2010). And
indeed, the “fishing down foodwebs” theory represents an overall
shift from long-lived piscivorous fish towards smaller herbivorous
and planktivorous groups (Pauly et al., 1998, 2002). Why then are
seabird populations expected to decline because of the overexploitation of tuna stocks? Forage fish species usually remain within surface
waters (≤50 m), but few tropical seabird species are able to dive
deeper than a few metres (≤10 m) below the surface (Le Corre,
1997; Ballance and Pitman, 1999; Peck and Cogdon, 2006).
Consequently, most of these birds forage in mixed-species flocks
that are often associated with marine mammals and surface-feeding
tunas (Ballance and Pitman, 1999; Jaquemet et al., 2004; Le Corre
and Jaquemet, 2005). Various authors have even demonstrated
that little tropical seabird feeding activity occurs in the absence
of these subsurface predator groups (Harrison and Seki, 1987;
Le Corre and Jaquemet, 2005), and most birds appear to actively
search for mixed species flocks that signify the feeding frenzies
from which most resources are gathered. Therefore, declines in
tuna populations imply that the “new” forage fish stocks would be
largely unavailable to the seabirds, ultimately resulting in declines
in bird populations’ (Baum and Worm, 2009).
To estimate how far subsurface predator populations would need
to decline before there are serious effects on seabird foraging would
require accurate stock estimates of predatory and forage fish with
which to make a temporal comparison against the declining
seabird populations. Forage fish stock estimates currently do not
exist for the region, as these groups are rarely targeted by the
fishing industry in this area, so that we cannot compare the relative
offtake by humans (i.e. fisheries) and seabirds. Tuna and billfish
stock estimates are available from the IOTC but are based on
catch per unit effort (cpue) data and we have to assume that they
are not biased or underreported in any way. Furthermore, various
authors have now questioned the use of cpue data as they often
present a misleading picture of the status of large predatory fish
2596
(Watson and Pauly, 2001; Maunder et al., 2006; Polacheck, 2006).
Though it is clear that predatory fish stocks are only a fraction of
their historical levels (Myers and Worm, 2003; Pauly et al., 2003;
Srinivasan et al., 2010; Juan-Jordá et al., 2011), the IOTC believe
that, at least for most species, quotas are still well within sustainable
levels however.
Tropical seabirds are surface foragers so that the longline catches,
which are usually dominated by swordfish and mature tunas that
rarely feed at the surface, may not immediately affect seabird
access to their prey. Furthermore, the risk of bycatch is low in the
tropics, compared with higher latitudes, as no tropical seabirds actively scavenge behind fishing vessels. Nevertheless, the exploitation
of mature tuna by longliners does have the potential to influence
tuna population dynamics and indirectly affecting these seabirds.
On the other hand, purse-seine fishing, which is by far the dominant
fishing type in the region, targets schools of juvenile tuna with which
the seabirds regularly interact at the surface so that we anticipate the
effects of purse-seine fishing on seabird populations to be much
greater. Furthermore, the spatial overlap between the habitats
used by seabirds, during the breeding season, and purse-seine
fishing is higher than for longlining, suggesting that the immediate
impacts of this fishing type will be much greater.
Implications for conservation
Seabird populations in the WIO are thought to be a fraction of the
historical estimates. Many colonies have become extinct and those
that still exist are greatly reduced in size (Feare, 1978; Cheke,
2001; Feare et al., 2007). Feare (1978) recognized that one of the
main conservation priorities for the WIO was to survey the remaining seabird breeding colonies and to identify and monitor the local
factors that might influence these populations. While considerable
scientific attention has been devoted to understanding the threats
these birds might face on land, little is known about the perturbations they experience at sea. Fisheries pose some of the greatest
threats to seabirds today and the overexploitation of marine fish
stocks has greatly affected seabird populations worldwide (Tasker
et al., 2000). Various tools are now available that promote EBFM
in an effective manner and one of the most commonly employed
methods is that of Marine Protected Areas (MPAs). MPAs are
being introduced worldwide with the primary aim of enhancing
fish stocks and conserving marine biodiversity (Buxton et al.,
2006; Turpie et al., 2006; Worm et al., 2009). Offshore (pelagic)
MPAs could benefit species targeted by fisheries, while also
helping to sustain fishery practices over time (Worm et al., 2009;
Le Corre et al., 2012). Turpie et al. (2006) found that the value of
MPAs far exceeds the revenue that these areas would have generated
if unprotected and by linking MPAs in coherent networks, ecosystem recovery, and conservation can be promoted supporting
wider management issues. Despite this, MPAs cover ,1% of all
marine ecosystems and few other tools are available that protect ecosystem integrity in such an effective manner (Roberts et al., 2005;
Worm et al., 2009).
Some attempt has been made to identify areas suitable for protection in the WIO; however, little policy response has been achieved
yet (Le Corre et al., 2012). Various MPAs have been implemented
in the region, but most of these are designed to protect fringing/
coastal ecosystems and, except the areas around the Chagos
Archipelago, pelagic communities remain largely unprotected
(Koldewey et al., 2010; Le Corre et al., 2012). Since most seabird
species in the WIO are pelagic foragers, they are unlikely to
receive any direct benefits from this form of protection. Many
D. K. Danckwerts et al.
colonies have also been labelled Important Bird Areas but, again,
this does not necessarily imply that the birds are protected while
at sea (Fishpool and Evans, 2001).
Cury et al. (2011) also demonstrated that, in several ecosystems
where seabirds are strongly dependent on forage species (small
coastal pelagic fish, euphausiids, or squid), a practical way to
sustain healthy upper trophic level predator populations and ecosystem functions would be to maintain forage fish biomass above
one-third of the maximum observed long-term biomass. In the
WIO, seabirds are widely used by fishers to find surface tuna
schools. It will be of great interest to quantify the real dependence
of seabirds on tuna to define a threshold of exploitation that
would not affect seabird population dynamics, as this could contribute to effective EBFM.
Supplementary data
Supplementary material is available at the ICESJMS online version
of the manuscript.
Acknowledgements
The first author would like to personally thank T. Diamond, P. Carr,
S. Geelhoed, S. Muzaffar, M. Villet, W. Froneman, H. Retief, and
K.L. Kelly for their assistance and seemingly endless support
during various phases of this research. This work is based upon research supported by the South African Research Chairs Initiative of
the Department of Science and Technology and the National
Research Foundation. We also thank the two anonymous referees
and the editor for their insightful comments, critiques, and
suggestions that led to the production of the final version of this
manuscript.
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Handling editor: Kees Camphuysen