- Email: [email protected]
Seagrass beds and mangroves as potential nurseries for the threatened Indo-Pacific humphead wrasse, Cheilinus undulatus and Caribbean rainbow parrotfish, Scarus guacamaia
B I O L O G I CA L C O N S E RVAT I O N
1 2 9 ( 2 0 0 6 ) 2 7 7 –2 8 2
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/biocon
Short communication
Seagrass beds and mangroves as potential nurseries for the threatened Indo-Pacific humphead wrasse, Cheilinus undulatus and Caribbean rainbow parrotfish, Scarus guacamaia M. Dorenbosch, M.G.G. Grol, I. Nagelkerken*, G. van der Velde Department of Animal Ecology and Ecophysiology, Institute for Water and Wetland Research, Radboud University Nijmegen, Toernooiveld 1, 6525 ED, Nijmegen, The Netherlands
A R T I C L E I N F O
A B S T R A C T
Article history:
The importance of seagrass beds and mangroves as a juvenile habitat as opposed to other
Received 16 July 2005
shallow water habitat types is investigated using a single sampling method on four islands
Received in revised form
in the western Indian Ocean for Cheilinus undulatus, and on one island in the southern
11 October 2005
Caribbean Sea for Scarus guacamaia. Both species occur on the Red list of threatened spe-
Accepted 24 October 2005
cies. Juveniles of Cheilinus undulatus were predominantly found on seagrass beds while
Available online 15 December 2005
adults were limited to the coral reef. The presence of seagrass beds resulted in significantly higher densities of the species on coral reefs in front of these habitats, indicating the
Keywords:
importance of seagrass beds as a juvenile habitat. For Scarus guacamaia, juveniles were
Coral reef fishes
exclusively observed in mangroves while adults only occurred on the coral reef. Adult S.
Nursery
guacamaia occurred on all coral reefs along the sheltered coast of the island containing
Seagrass beds
mangroves, but no relationship with distance to mangroves was observed. This could indi-
Mangroves
cate the importance of mangroves for the occurrence of adults of this species on the scale
Conservation
of an entire island. Ó 2005 Elsevier Ltd. All rights reserved.
1.
Introduction
Seagrass beds and mangroves are thought to function as important nurseries for many coral reef fish species (Parrish, 1989; Robertson and Blaber, 1992; Beck et al., 2001). This nursery hypothesis is an essential argument for the conservation of these habitats with respect to coral reef fishes. However, the number of studies that compare the value of these habitats as a juvenile habitat with the value of other possible shallow water habitats and the coral reef itself, is still limited. The present study focuses on the habitat utilization of two of the largest coral reef fishes in the world, Cheilinus undulatus and
Scarus guacamaia. Cheilinus undulatus is considered a threatened fish of the world (Donaldson and Sadovy, 2001) and is listed on Appendix II of CITES (2004) whereas both species occur on the IUCN Red list of threatened species (IUCN 2004). Cheilinus undulatus is the largest species of Labridae and occurs in the Indo-Pacific region. Adults are associated with coral reefs while juveniles have been reported from various lagoon habitats such as shallow corals and seagrass beds (Randall et al., 1978; Sadovy et al., 2003). However, studies are lacking that quantitatively investigated the use of shallow water habitats by juveniles of this species. Scarus guacamaia is the largest herbivorous coral reef fish that occurs in the Caribbean region.
* Corresponding author: Tel.: +31 243652471. E-mail address: [email protected] (I. Nagelkerken). 0006-3207/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2005.10.032
278
B I O L O G I C A L C O N S E RVAT I O N
Although juveniles are thought to be associated with mangrove habitats, only two studies quantitatively demonstrated the importance of mangroves as a juvenile habitat as opposed to seagrass beds and the coral reef (Nagelkerken et al., 2000; Mumby et al., 2004). Both Cheilinus undulatus and Scarus guacamaia can attain a high biomass and have a high commercial value for fisheries. Using one sampling method in both tropical regions, we investigate the importance of seagrass beds and
1 2 9 ( 2 0 0 6 ) 2 7 7 –2 8 2
mangroves as a juvenile habitat as opposed to all other available main shallow water habitats.
2.
Methodology
Using underwater visual census in stationary point count transects (Polunin and Roberts, 1993), we investigated the occurrence and densities of Cheilinus undulatus in six major
Fig. 1 – Location of the four investigated islands off the coast of Tanzania, western Indian Ocean, where Cheilinus undulatus was observed (a), and the island of Aruba, southern Caribbean Sea, where Scarus guacamaia was observed (b). Geographic location island of Zanzibar: 6°10 0 S, 39°10 0 E.
B I O L O G I C A L C O N S E RVAT I O N
279
1 2 9 ( 2 0 0 6 ) 2 7 7 –2 8 2
Table 1 – Surveyed habitat types, number of sites, transects and transect sizes on the islands of the coast off Tanzania, western Indian Ocean (Cheilinus undulatus) and the island of Aruba, southern Caribbean Sea (Scarus guacamaia) # Transects
Surveyed habitats Cheilinus undulatus, Tanzania Seagrass beds Macro-algal flats Intertidal flats Notches Mangrove prop-roots Seagrass–mangrove reefs Far reefs Surveyed habitats Scarus guacamaia, Aruba: Notches Seagrass beds Mangrove prop-roots Coral reefs
388 126 268 35 67 730 1582
29 201 81 483
Transect Total surveyed size (m2) surface (m2)
25 25 25 15 25 25/64 64
Aruba Mafia Mbudya Zanzibar Pemba
9700 3150 6700 525 1675 31 003 101 248
15 25 10 100
coastal marine habitats on four islands near the coast of Tanzania, western Indian Ocean (i.e., Mafia, Mbudya, Pemba and Zanzibar, Fig. 1): seagrass beds, macro-algal flats, intertidal flats characterized by patches of seagrass and corals, notches (i.e., overhanging rocks forming small caverns along a fossilized limestone shore line), mangrove prop-roots and coral reefs (Table 1 and Fig. 1). Two types of coral reefs were distinguished, viz., coral reefs that were located in front of lagoons with seagrass beds and mangroves (seagrass–mangrove reefs) and coral reefs that were located far away from seagrass beds and mangroves (far reefs, mean distance to seagrass beds or mangroves was 17.2 km). For Scarus guacamaia, we investigated the occurrence and densities of the four most important coastal habitats on the island of Aruba (Caribbean Sea): seagrass beds, mangrove prop-roots, notches and coral reefs (Table 1 and Fig. 1). Coral reefs (n = 13) were located along the entire coast of the island and were arranged in a continuous distance gradient to mangroves that were exclusively located on the sheltered southwestern side of the island. The shortest distance between a coral reef site and mangroves was 250 m whereas the longest distance between a coral reef site and mangroves was 26 km. SCUBA was used to survey all coral reefs and the seagrass beds. Transects on coral reefs were surveyed at water depths between 3 and 20 m, on seagrass beds between 2 and 4 m. For all mangroves, notches, macro-algal and intertidal flats, and seagrass beds located on Aruba, snorkeling gear was used instead of SCUBA because of the limited depth of these habitats (between 1.5 and 3 m). Because underwater visibility varied between habitat types, transect sizes ranged between 20 and 100 m2. Information on the number of surveyed sites and the surface area and number of surveyed transects are presented in Table 1. In each transect, observers counted fishes during ten minutes. Fish size was estimated in size classes of 2.5 cm (total length) for fishes <30 cm, whereas for fishes 30–50 cm and >50 cm total length was estimated to the nearest 10 cm and 20 cm, respectively. Estimation of size classes was first thoroughly practiced simultaneously by the observers (Tanzania: 4 observers, Aruba: 2 observers). Data for Cheilinus undulatus were collected in 2003, for Scarus guacamaia in 2004.
# of surveyed sites per island
435 5025 810 48300
4
1 4 2
1 1
10 2 2 1 1 10 6
2
2 2 3
1 3 4 13
To investigate the effect of the presence of lagoons containing seagrass beds and mangroves on total fish density on the coral reef, total fish densities of Cheilinus undulatus were compared between seagrass–mangrove reefs and far reefs. Differences in densities were tested using Poisson regression models fitted using the GENMOD procedure (SAS Institute Inc., 1993). Data were corrected for overdispersion, the different coral reef sites were nested within the two coral reef types and significance of the relationship was tested using Wald v2 statistic. For Scarus guacamaia, the relationship between total fish density on the coral reef and shortest geographic distance to mangroves was determined using linear regression analysis.
3.
Results
Of all available habitat types, both species were exclusively observed in only two habitat types. Cheilinus undulatus was only observed on seagrass beds and coral reefs, where 170 individuals were counted with sizes ranging between 2.5 and 120 cm. All individuals observed on seagrass beds were <27.5 cm whereas 75% of the observed individuals on the coral reef were >27.5 cm (Fig. 2a). Sizes of C. undulatus on seagrass–mangrove reefs ranged between 5 and 130 cm, on far reefs between 10 and 110 cm. Mean total density of C. undulatus on seagrass– mangrove reefs (0.19 ± 0.43 100 m2 ± SD) was significantly higher than on far reefs (0.05 ± 0.27 100 m2 ± SD, P < 0.001, coral reef sites had a significant nesting effect, P < 0.001). Scarus guacamaia was only observed in mangroves and on coral reefs, where 205 individuals were counted with sizes ranging between 5 and 80 cm. Mangroves exclusively harboured individuals <30 cm whereas all individuals of this species observed on the coral reef were >25 cm (Fig. 2b). All adult individuals of S. guacamaia were observed on coral reefs located on the sheltered southwestern side of the island where most individuals were observed on coral reefs between 0 and 10 km distance from mangroves (Fig. 3, maximum distance between coral reefs where the species was observed and mangroves was 13 km). The species was completely absent from the two coral reefs located farthest away from mangroves, on the exposed northeastern side of the island
280
B I O L O G I C A L C O N S E RVAT I O N
1 2 9 ( 2 0 0 6 ) 2 7 7 –2 8 2
Fig. 2 – Size frequency distribution of Cheilinus undulatus (a) and Scarus guacamaia (b) on the investigated habitats. Scale bar on right-hand y-axis represents densities on the coral reef.
(located at 17 and 26 km distance to the nearest mangroves, Fig. 1). No significant linear relationship was present between mean total density of S. guacamaia on these reefs and distance to nearest mangroves (R2 = 0.01; P = 0.827).
4.
Discussion
The results of the present study indicate ontogenetic shifts from juvenile habitats (seagrass beds for Cheilinus undulatus
B I O L O G I C A L C O N S E RVAT I O N
1 2 9 ( 2 0 0 6 ) 2 7 7 –2 8 2
281
40
# of observed adults
35 30 25 20 15 10 5 0 0-1
1-5
5 - 10
> 10
Distance to nearest mangroves (km) Fig. 3 – Relationship between the total number of adult Scarus guacamaia observed on coral reefs and the shortest distance to mangroves. and mangroves for Scarus guacamaia) towards adult habitats (coral reefs). Cheilinus undulatus may also use the coral reef as a juvenile habitat (Randall et al., 1978; personal communications listed in Sadovy et al., 2003), but the present study shows seagrass beds form the most important juvenile habitat on the four investigated islands. The results indicate that the presence of lagoons with seagrass beds subsequently enhance the adult densities of the species on coral reefs in front of these habitats. Seagrass beds may therefore play an important role in conservation of adult fish stocks of this species on adjacent coral reefs. For Scarus guacamaia, juveniles were exclusively observed in mangroves. The present study focused on a new geographic area and included higher numbers of fish compared with previous studies. In combination with results of Nagelkerken et al. (2000) and Mumby et al. (2004) it can therefore be suggested mangroves may be the single most important juvenile habitat for this species. On the scale of the island of Aruba, the species was observed on coral reefs along the entire sheltered southwest coast. Since mangroves were the only habitat where juveniles were observed, the presence of mangroves is likely to be an essential factor for the occurrence of Scarus guacamaia along the entire sheltered coast of the island. As has been suggested by Mumby et al. (2004), loss of mangrove habitat could therefore affect adult populations on coral reefs situated far away from this habitat (in the present study possibly up to 10 km). Measures aimed at the conservation of threatened species such as Cheilinus undulatus and Scarus guacamaia, should therefore also be aimed at shallow water habitats such as seagrass beds and mangroves that are likely to function as important juvenile habitats.
Acknowledgments This study was funded by the Department of Agriculture and Fisheries (DAF) of the island of Aruba, and by Nuffic through the ENVIRONS – MHO programme. Fly and Dive Aruba provided all diving facilities on Aruba, Sensation Divers on Zan-
zibar, Swahili Divers on Pemba, and Mafia Marine Park on Mafia. We thank the staff and personnel of DAF (Aruba), and of the Institute of Marine Sciences (Zanzibar, Tanzania) for their logistic support and facilities. G. Atsma, J. Bosman, M. Christianen, V. de Jong, T. Kolbrink, and A. Pustjens assisted during the fieldwork. P. Portier provided important logistic support during the field research on Aruba. This is Centre for Wetland Ecology publication no. 414.
R E F E R E N C E S
Beck, M.W., Heck, K.L., Able, K.W., Childers, D.L., Eggleston, D.B., Gillanders, B.M., Halpern, B., Hays, C.G., Hoshino, K., Minello, T.J., Orth, R.J., Sheridan, P.F., Weinstein, M.P., 2001. The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bioscience 51, 633–641. Convention on International Trade in Endangered Species, 2004. Species Listing Changes Adopted at the 13th Conference of the Parties to the Convention on International Trade in Endangered Species (CITES). Electronic version available on http://www.cites.org. International Union for Conservation of Nature and Natural Resources, 2004. 2004 IUCN Red List of Threatened Species. Electronic version available on http://www.redlist/org. Donaldson, T.J., Sadovy, Y., 2001. Threatened fishes of the world: Cheilinus undulatus Ru¨ppell, 1835 (Labridae). Environmental Biology of Fishes 62, 428. Mumby, P.J., Edwards, A.J., Arias-Gonzalez, J.E., Lindeman, P.G., Blackwell, K.G., Gall, A., Gorczynska, M.I., Harborne, A.R., Pescod, C.L., Renken, H., Wabnitz, C.C.C., Llewellyn, G., 2004. Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427, 533–536. Nagelkerken, I., Dorenbosch, M., Verberk, W.C.E.P., Cocheret de la Morinie`re, E., van der Velde, G., 2000. Importance of shallow-water biotopes of a Caribbean bay for juvenile coral reef fishes: patterns in biotope association, community structure and spatial distribution. Marine Ecology Progress Series 202, 175–193. Parrish, J.D., 1989. Fish communities of interacting shallow-water habitats in tropical oceanic regions. Marine Ecology Progress Series 58, 143–160.
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Polunin, N.V.C., Roberts, C.M., 1993. Greater biomass and value of target coral-reef fishes in two small Caribbean marine reserves. Marine Ecology Progress Series 100, 167–176. Randall, J.E., Head, S.M., Sanders, A.P.L., 1978. Food habits of the giant humphead wrasse Cheilinus undulatus (Labridae). Environmental Biology of Fishes 3, 235–238. Robertson, A.I., Blaber, S.J.M., 1992. Plankton, epibenthos and fish communities. In: Robertson, A.I., Alongi, D.M. (Eds.), Tropical
1 2 9 ( 2 0 0 6 ) 2 7 7 –2 8 2
Mangrove Ecosystems, Coastal and Estuarine Studies, vol. 41. American Geophysical Union, Washington, DC, pp. 173–224. Sadovy, Y., Kulbicki, M., Labrosse, P., Letourneur, Y., Lokani, P., Donaldson, T.J., 2003. The humphead wrasse, Cheilinus undulatus: synopsis of a threatened and poorly known giant coral reef. Reviews in Fish Biology and Fisheries 13, 327–364. SAS Institute Inc., 1993. SAS/STATTM software: the GENMOD procedure. Tech. Rep. p 243 of the SAS Institute Inc., Cary, NC.
1 2 9 ( 2 0 0 6 ) 2 7 7 –2 8 2
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/biocon
Short communication
Seagrass beds and mangroves as potential nurseries for the threatened Indo-Pacific humphead wrasse, Cheilinus undulatus and Caribbean rainbow parrotfish, Scarus guacamaia M. Dorenbosch, M.G.G. Grol, I. Nagelkerken*, G. van der Velde Department of Animal Ecology and Ecophysiology, Institute for Water and Wetland Research, Radboud University Nijmegen, Toernooiveld 1, 6525 ED, Nijmegen, The Netherlands
A R T I C L E I N F O
A B S T R A C T
Article history:
The importance of seagrass beds and mangroves as a juvenile habitat as opposed to other
Received 16 July 2005
shallow water habitat types is investigated using a single sampling method on four islands
Received in revised form
in the western Indian Ocean for Cheilinus undulatus, and on one island in the southern
11 October 2005
Caribbean Sea for Scarus guacamaia. Both species occur on the Red list of threatened spe-
Accepted 24 October 2005
cies. Juveniles of Cheilinus undulatus were predominantly found on seagrass beds while
Available online 15 December 2005
adults were limited to the coral reef. The presence of seagrass beds resulted in significantly higher densities of the species on coral reefs in front of these habitats, indicating the
Keywords:
importance of seagrass beds as a juvenile habitat. For Scarus guacamaia, juveniles were
Coral reef fishes
exclusively observed in mangroves while adults only occurred on the coral reef. Adult S.
Nursery
guacamaia occurred on all coral reefs along the sheltered coast of the island containing
Seagrass beds
mangroves, but no relationship with distance to mangroves was observed. This could indi-
Mangroves
cate the importance of mangroves for the occurrence of adults of this species on the scale
Conservation
of an entire island. Ó 2005 Elsevier Ltd. All rights reserved.
1.
Introduction
Seagrass beds and mangroves are thought to function as important nurseries for many coral reef fish species (Parrish, 1989; Robertson and Blaber, 1992; Beck et al., 2001). This nursery hypothesis is an essential argument for the conservation of these habitats with respect to coral reef fishes. However, the number of studies that compare the value of these habitats as a juvenile habitat with the value of other possible shallow water habitats and the coral reef itself, is still limited. The present study focuses on the habitat utilization of two of the largest coral reef fishes in the world, Cheilinus undulatus and
Scarus guacamaia. Cheilinus undulatus is considered a threatened fish of the world (Donaldson and Sadovy, 2001) and is listed on Appendix II of CITES (2004) whereas both species occur on the IUCN Red list of threatened species (IUCN 2004). Cheilinus undulatus is the largest species of Labridae and occurs in the Indo-Pacific region. Adults are associated with coral reefs while juveniles have been reported from various lagoon habitats such as shallow corals and seagrass beds (Randall et al., 1978; Sadovy et al., 2003). However, studies are lacking that quantitatively investigated the use of shallow water habitats by juveniles of this species. Scarus guacamaia is the largest herbivorous coral reef fish that occurs in the Caribbean region.
* Corresponding author: Tel.: +31 243652471. E-mail address: [email protected] (I. Nagelkerken). 0006-3207/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2005.10.032
278
B I O L O G I C A L C O N S E RVAT I O N
Although juveniles are thought to be associated with mangrove habitats, only two studies quantitatively demonstrated the importance of mangroves as a juvenile habitat as opposed to seagrass beds and the coral reef (Nagelkerken et al., 2000; Mumby et al., 2004). Both Cheilinus undulatus and Scarus guacamaia can attain a high biomass and have a high commercial value for fisheries. Using one sampling method in both tropical regions, we investigate the importance of seagrass beds and
1 2 9 ( 2 0 0 6 ) 2 7 7 –2 8 2
mangroves as a juvenile habitat as opposed to all other available main shallow water habitats.
2.
Methodology
Using underwater visual census in stationary point count transects (Polunin and Roberts, 1993), we investigated the occurrence and densities of Cheilinus undulatus in six major
Fig. 1 – Location of the four investigated islands off the coast of Tanzania, western Indian Ocean, where Cheilinus undulatus was observed (a), and the island of Aruba, southern Caribbean Sea, where Scarus guacamaia was observed (b). Geographic location island of Zanzibar: 6°10 0 S, 39°10 0 E.
B I O L O G I C A L C O N S E RVAT I O N
279
1 2 9 ( 2 0 0 6 ) 2 7 7 –2 8 2
Table 1 – Surveyed habitat types, number of sites, transects and transect sizes on the islands of the coast off Tanzania, western Indian Ocean (Cheilinus undulatus) and the island of Aruba, southern Caribbean Sea (Scarus guacamaia) # Transects
Surveyed habitats Cheilinus undulatus, Tanzania Seagrass beds Macro-algal flats Intertidal flats Notches Mangrove prop-roots Seagrass–mangrove reefs Far reefs Surveyed habitats Scarus guacamaia, Aruba: Notches Seagrass beds Mangrove prop-roots Coral reefs
388 126 268 35 67 730 1582
29 201 81 483
Transect Total surveyed size (m2) surface (m2)
25 25 25 15 25 25/64 64
Aruba Mafia Mbudya Zanzibar Pemba
9700 3150 6700 525 1675 31 003 101 248
15 25 10 100
coastal marine habitats on four islands near the coast of Tanzania, western Indian Ocean (i.e., Mafia, Mbudya, Pemba and Zanzibar, Fig. 1): seagrass beds, macro-algal flats, intertidal flats characterized by patches of seagrass and corals, notches (i.e., overhanging rocks forming small caverns along a fossilized limestone shore line), mangrove prop-roots and coral reefs (Table 1 and Fig. 1). Two types of coral reefs were distinguished, viz., coral reefs that were located in front of lagoons with seagrass beds and mangroves (seagrass–mangrove reefs) and coral reefs that were located far away from seagrass beds and mangroves (far reefs, mean distance to seagrass beds or mangroves was 17.2 km). For Scarus guacamaia, we investigated the occurrence and densities of the four most important coastal habitats on the island of Aruba (Caribbean Sea): seagrass beds, mangrove prop-roots, notches and coral reefs (Table 1 and Fig. 1). Coral reefs (n = 13) were located along the entire coast of the island and were arranged in a continuous distance gradient to mangroves that were exclusively located on the sheltered southwestern side of the island. The shortest distance between a coral reef site and mangroves was 250 m whereas the longest distance between a coral reef site and mangroves was 26 km. SCUBA was used to survey all coral reefs and the seagrass beds. Transects on coral reefs were surveyed at water depths between 3 and 20 m, on seagrass beds between 2 and 4 m. For all mangroves, notches, macro-algal and intertidal flats, and seagrass beds located on Aruba, snorkeling gear was used instead of SCUBA because of the limited depth of these habitats (between 1.5 and 3 m). Because underwater visibility varied between habitat types, transect sizes ranged between 20 and 100 m2. Information on the number of surveyed sites and the surface area and number of surveyed transects are presented in Table 1. In each transect, observers counted fishes during ten minutes. Fish size was estimated in size classes of 2.5 cm (total length) for fishes <30 cm, whereas for fishes 30–50 cm and >50 cm total length was estimated to the nearest 10 cm and 20 cm, respectively. Estimation of size classes was first thoroughly practiced simultaneously by the observers (Tanzania: 4 observers, Aruba: 2 observers). Data for Cheilinus undulatus were collected in 2003, for Scarus guacamaia in 2004.
# of surveyed sites per island
435 5025 810 48300
4
1 4 2
1 1
10 2 2 1 1 10 6
2
2 2 3
1 3 4 13
To investigate the effect of the presence of lagoons containing seagrass beds and mangroves on total fish density on the coral reef, total fish densities of Cheilinus undulatus were compared between seagrass–mangrove reefs and far reefs. Differences in densities were tested using Poisson regression models fitted using the GENMOD procedure (SAS Institute Inc., 1993). Data were corrected for overdispersion, the different coral reef sites were nested within the two coral reef types and significance of the relationship was tested using Wald v2 statistic. For Scarus guacamaia, the relationship between total fish density on the coral reef and shortest geographic distance to mangroves was determined using linear regression analysis.
3.
Results
Of all available habitat types, both species were exclusively observed in only two habitat types. Cheilinus undulatus was only observed on seagrass beds and coral reefs, where 170 individuals were counted with sizes ranging between 2.5 and 120 cm. All individuals observed on seagrass beds were <27.5 cm whereas 75% of the observed individuals on the coral reef were >27.5 cm (Fig. 2a). Sizes of C. undulatus on seagrass–mangrove reefs ranged between 5 and 130 cm, on far reefs between 10 and 110 cm. Mean total density of C. undulatus on seagrass– mangrove reefs (0.19 ± 0.43 100 m2 ± SD) was significantly higher than on far reefs (0.05 ± 0.27 100 m2 ± SD, P < 0.001, coral reef sites had a significant nesting effect, P < 0.001). Scarus guacamaia was only observed in mangroves and on coral reefs, where 205 individuals were counted with sizes ranging between 5 and 80 cm. Mangroves exclusively harboured individuals <30 cm whereas all individuals of this species observed on the coral reef were >25 cm (Fig. 2b). All adult individuals of S. guacamaia were observed on coral reefs located on the sheltered southwestern side of the island where most individuals were observed on coral reefs between 0 and 10 km distance from mangroves (Fig. 3, maximum distance between coral reefs where the species was observed and mangroves was 13 km). The species was completely absent from the two coral reefs located farthest away from mangroves, on the exposed northeastern side of the island
280
B I O L O G I C A L C O N S E RVAT I O N
1 2 9 ( 2 0 0 6 ) 2 7 7 –2 8 2
Fig. 2 – Size frequency distribution of Cheilinus undulatus (a) and Scarus guacamaia (b) on the investigated habitats. Scale bar on right-hand y-axis represents densities on the coral reef.
(located at 17 and 26 km distance to the nearest mangroves, Fig. 1). No significant linear relationship was present between mean total density of S. guacamaia on these reefs and distance to nearest mangroves (R2 = 0.01; P = 0.827).
4.
Discussion
The results of the present study indicate ontogenetic shifts from juvenile habitats (seagrass beds for Cheilinus undulatus
B I O L O G I C A L C O N S E RVAT I O N
1 2 9 ( 2 0 0 6 ) 2 7 7 –2 8 2
281
40
# of observed adults
35 30 25 20 15 10 5 0 0-1
1-5
5 - 10
> 10
Distance to nearest mangroves (km) Fig. 3 – Relationship between the total number of adult Scarus guacamaia observed on coral reefs and the shortest distance to mangroves. and mangroves for Scarus guacamaia) towards adult habitats (coral reefs). Cheilinus undulatus may also use the coral reef as a juvenile habitat (Randall et al., 1978; personal communications listed in Sadovy et al., 2003), but the present study shows seagrass beds form the most important juvenile habitat on the four investigated islands. The results indicate that the presence of lagoons with seagrass beds subsequently enhance the adult densities of the species on coral reefs in front of these habitats. Seagrass beds may therefore play an important role in conservation of adult fish stocks of this species on adjacent coral reefs. For Scarus guacamaia, juveniles were exclusively observed in mangroves. The present study focused on a new geographic area and included higher numbers of fish compared with previous studies. In combination with results of Nagelkerken et al. (2000) and Mumby et al. (2004) it can therefore be suggested mangroves may be the single most important juvenile habitat for this species. On the scale of the island of Aruba, the species was observed on coral reefs along the entire sheltered southwest coast. Since mangroves were the only habitat where juveniles were observed, the presence of mangroves is likely to be an essential factor for the occurrence of Scarus guacamaia along the entire sheltered coast of the island. As has been suggested by Mumby et al. (2004), loss of mangrove habitat could therefore affect adult populations on coral reefs situated far away from this habitat (in the present study possibly up to 10 km). Measures aimed at the conservation of threatened species such as Cheilinus undulatus and Scarus guacamaia, should therefore also be aimed at shallow water habitats such as seagrass beds and mangroves that are likely to function as important juvenile habitats.
Acknowledgments This study was funded by the Department of Agriculture and Fisheries (DAF) of the island of Aruba, and by Nuffic through the ENVIRONS – MHO programme. Fly and Dive Aruba provided all diving facilities on Aruba, Sensation Divers on Zan-
zibar, Swahili Divers on Pemba, and Mafia Marine Park on Mafia. We thank the staff and personnel of DAF (Aruba), and of the Institute of Marine Sciences (Zanzibar, Tanzania) for their logistic support and facilities. G. Atsma, J. Bosman, M. Christianen, V. de Jong, T. Kolbrink, and A. Pustjens assisted during the fieldwork. P. Portier provided important logistic support during the field research on Aruba. This is Centre for Wetland Ecology publication no. 414.
R E F E R E N C E S
Beck, M.W., Heck, K.L., Able, K.W., Childers, D.L., Eggleston, D.B., Gillanders, B.M., Halpern, B., Hays, C.G., Hoshino, K., Minello, T.J., Orth, R.J., Sheridan, P.F., Weinstein, M.P., 2001. The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bioscience 51, 633–641. Convention on International Trade in Endangered Species, 2004. Species Listing Changes Adopted at the 13th Conference of the Parties to the Convention on International Trade in Endangered Species (CITES). Electronic version available on http://www.cites.org. International Union for Conservation of Nature and Natural Resources, 2004. 2004 IUCN Red List of Threatened Species. Electronic version available on http://www.redlist/org. Donaldson, T.J., Sadovy, Y., 2001. Threatened fishes of the world: Cheilinus undulatus Ru¨ppell, 1835 (Labridae). Environmental Biology of Fishes 62, 428. Mumby, P.J., Edwards, A.J., Arias-Gonzalez, J.E., Lindeman, P.G., Blackwell, K.G., Gall, A., Gorczynska, M.I., Harborne, A.R., Pescod, C.L., Renken, H., Wabnitz, C.C.C., Llewellyn, G., 2004. Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427, 533–536. Nagelkerken, I., Dorenbosch, M., Verberk, W.C.E.P., Cocheret de la Morinie`re, E., van der Velde, G., 2000. Importance of shallow-water biotopes of a Caribbean bay for juvenile coral reef fishes: patterns in biotope association, community structure and spatial distribution. Marine Ecology Progress Series 202, 175–193. Parrish, J.D., 1989. Fish communities of interacting shallow-water habitats in tropical oceanic regions. Marine Ecology Progress Series 58, 143–160.
282
B I O L O G I C A L C O N S E RVAT I O N
Polunin, N.V.C., Roberts, C.M., 1993. Greater biomass and value of target coral-reef fishes in two small Caribbean marine reserves. Marine Ecology Progress Series 100, 167–176. Randall, J.E., Head, S.M., Sanders, A.P.L., 1978. Food habits of the giant humphead wrasse Cheilinus undulatus (Labridae). Environmental Biology of Fishes 3, 235–238. Robertson, A.I., Blaber, S.J.M., 1992. Plankton, epibenthos and fish communities. In: Robertson, A.I., Alongi, D.M. (Eds.), Tropical
1 2 9 ( 2 0 0 6 ) 2 7 7 –2 8 2
Mangrove Ecosystems, Coastal and Estuarine Studies, vol. 41. American Geophysical Union, Washington, DC, pp. 173–224. Sadovy, Y., Kulbicki, M., Labrosse, P., Letourneur, Y., Lokani, P., Donaldson, T.J., 2003. The humphead wrasse, Cheilinus undulatus: synopsis of a threatened and poorly known giant coral reef. Reviews in Fish Biology and Fisheries 13, 327–364. SAS Institute Inc., 1993. SAS/STATTM software: the GENMOD procedure. Tech. Rep. p 243 of the SAS Institute Inc., Cary, NC.