sm82n2-4683

Seasonality of planktonic crustacean decapod larvae in the subtropical waters of Gran Canaria Island, NE Atlantic

José M. Landeira 1, Fernando Lozano-Soldevilla 2

1 Department of Ocean Sciences, Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato, Tokyo 108-8477, Japan.
(JML) (Corresponding author) E-mail: jm_landeira@yahoo.es. ORCID ID: http://orcid.org/0000-0001-6419-2046
2 Departamento de Biología Animal, Edafología y Geología. Universidad de La Laguna, Avd. Astrofísico Francisco Sánchez, s/n. 38200 La Laguna, Spain.
(FL-S) E-mail: flozano@ull.edu.es. ORCID ID: http://orcid.org/0000-0002-1028-4356

Summary: A monitoring programme was established to collect plankton samples and information of environmental variables over the shelf off the island of Gran Canaria during 2005 and 2006. It produced a detailed snapshot of the composition and seasonal assemblages of the decapod larvae community in this locality, in the subtropical waters of the Canary Islands (NE Atlantic), where information about crustacean phenology has been poorly studied. The larval community was mainly composed of benthic taxa, but the contribution of pelagic taxa was also significant. Infraorders Anomura (33.4%) and Caridea (32.8%) accounted for more than half the total collected larvae. High diversity, relatively low larval abundance throughout the year and weak seasonality characterized the annual cycle. However, in relation to the temporal dynamics of temperature, two distinct larval assemblages (cold and warm) were identified that correspond to periods of mixing and stratification of the water column. The results also indicate that larval release times and durations in the subtropical waters are earlier and longer than at other higher latitudes in the NE Atlantic. We detected the presence of larvae of six species that have not yet been reported from the Canary Islands (Pandalina brevirostris, Processa edulis, Necallianasa truncata, Parapenaeus longirostris, Crangon crangon, Nematopagurus longicornis). Finally, this study provides a baseline for future comparisons with respect to fishery pressure and climate variability in this subtropical region.

Keywords: decapod larvae; phenology; assemblages; temperature; subtropical waters; Canary Islands.

Estacionalidad de las larvas de crustáceos decápodos en las aguas subtropicales de la isla de Gran Canaria, Atlántico NE

Resumen: Durante 2005 y 2006 se estableció un monitoreo para recolectar muestras de plancton e información de las variables ambientales sobre la plataforma insular de Gran Canaria. Esto produjo una instantánea detallada de la composición y estacionalidad de las asociaciones de la comunidad de larvas de decápodos en las aguas subtropicales de esta localidad de las Islas Canarias (Atlántico NE), donde la información sobre la fenología de crustáceos está pobremente estudiada. La comunidad de larvas estuvo principalmente compuesta por taxones bentónicos, pero con una contribución significativa de taxones pelágicos. Los infraórdenes Anomura (33.4%) y Caridea (32.8%) representaron más de la mitad del total de las larvas recolectadas. Alta diversidad, relativamente baja abundancia de larvas a lo largo de todo el año, y débil estacionalidad caracterizaron el ciclo anual. Sin embargo, y relacionado con la dinámica temporal de la temperatura, dos asociaciones larvarias distintas (fría y cálida) fueron identificadas que correspondieron con periodos de mezcla y estratificación de la columna de agua. Los resultados también indican que la duración y periodos de liberación de larvas en las aguas subtropicales son más tempranos y largos en el tiempo en comparación con otras latitudes más altas en el Atlántico NE. Además, se detecta la presencia de larvas de seis especies que no han sido citadas con anterioridad para las Islas Canarias (Pandalina brevirostris, Processa edulis, Necallianasa truncata, Parapenaeus longirostris, Crangon crangon, Nematopagurus longicornis). Finalmente, este estudio supone un punto de referencia para futuras comparaciones en relación con la presión pesquera y la variabilidad climática en esta región subtropical.

Palabras clave: larvas de decápodos; fenología; temperatura; diversidad; aguas subtropicales; Islas Canarias.

Citation/Cómo citar este artículo: Landeira J.M., Lozano-Soldevilla F. 2018. Seasonality of planktonic crustacean decapod larvae in the subtropical waters of Gran Canaria island, NE Atlantic. Sci. Mar. 82(2): 119-134. https://doi.org/10.3989/scimar.04683.08A

Editor: J.A. Cuesta

Received: June 29, 2017. Accepted: March 19, 2018. Published: April 23, 2018.

Copyright: © 2018 CSIC. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0) License.

Contents

Summary
Resumen
Introduction
Materials and methods
Results
Discussion
Acknowledgements
References

INTRODUCTIONTop

A key component for ecosystem and fishery management is an understanding of the reproductive strategies adopted by crustacean decapods in response to physical and biological processes. Most decapods have complex life cycles in which they release larvae into the water column where, as plankton, they develop through larval stages and may be transported far from their parental populations or retained near them by specific oceanographic features and larval behaviour (Shanks 1995Shanks A.L. 1995. Mechanisms of cross-shelf dispersal of larval invertebrates and fish. In: McEdward L.R. (ed.) Ecology of Marine Invertebrate larvae, CRC Press, Boca Raton, F.L., pp. 323-367., Queiroga and Blanton 2005Queiroga H., Blanton J. 2005. Interactions between behaviour and physical forcing in the control of horizontal transport of decapod crustacean larvae. Adv. Mar. Biol. 47: 107-214., Jones et al. 2007Jones G.P., Srinivasan M., Alamany G.R. 2007. Population connectivity and conservation of marine biodiversity. Oceanography 20: 100-111.). Therefore, the seasonal occurrence of larvae in the plankton usually provides valuable insight into the phenology of decapods. Further, the planktonic stage is a critical phase and larval pool mortality can exceed 90%, constituting a bottleneck that limits the population size (White et al. 2014White J.W., Morgan S.G., Fisher J.L. 2014. Planktonic larval mortality rates are lower than widely expected. Ecology 95: 3344-3353.). Laboratory and field studies have shown that larval mortality is determined by predation, competition for food and space, disease, and environmental stresses such as temperature, salinity, low oxygen concentrations, pollution, and ultraviolet irradiation (Shanks 1995Shanks A.L. 1995. Mechanisms of cross-shelf dispersal of larval invertebrates and fish. In: McEdward L.R. (ed.) Ecology of Marine Invertebrate larvae, CRC Press, Boca Raton, F.L., pp. 323-367., Eckman 1996Eckman J.E. 1996. Closing the larval loop: linking larval ecology to the population dynamics of marine benthic invertebrates. J. Exp. Mar. Biol. Ecol. 200: 207-237.). Thus, many species have evolved elaborate behavioural and life history strategies that exploit favourable periods of the year (those best matching optimal niche requirements) for growth, and minimize exposure of sensitive larval stages to stressful conditions (Ji et al. 2010Ji R., Edwards M., Mackas D.I., et al. 2010. Marine plankton phenology and life history in a changing climate: current research and future directions. J. Plankton Res. 32: 1355-1368.). Physical and biological cues seem to be involved that trigger larval release, such as temperature increase (Shirley and Shirley 1989Shirley S.M., Shirley T.C. 1989. Interannual variability in density, timing and survival of Alaskan red king crab Paralithodes camtschatica larvae. Mar. Ecol. Prog. Ser. 54: 51-59.), phytoplankton blooms (Starr et al. 1990Starr M., Himmelman J., Therriault J. 1990. Direct coupling of marine invertebrate spawning with phytoplankton blooms. Science 247: 1071-1074.), daylight duration and tidal amplitude (Morgan and Anastasia 2008Morgan S.G., Anastasia J.R. 2008. Behavioral tradeoff in estuarine larvae favors seaward migration over minimizing visibility to predators. Proc. Natl. Acad. Sci. USA 105: 222-227.). In general, the annual cycle of decapod larvae in temperate waters of NE Atlantic is related to the temperature regime, and seems to be linked to phytoplankton blooms (Kirby et al. 2008Kirby R., Beaugrand G., Lindley J.A. 2008. Climate-induced effects on the meroplankton and the benthic-pelagic ecology of the North Sea. Limnol. Oceanogr. 53: 1805-1815.), with two main abundance peaks during spring and summer (Highfield et al. 2010Highfield J.M., Eloire D., Conway D.V.P., et al. 2010. Seasonal dynamics of meroplankton assemblages at station L4. J. Plankton Res. 32: 681-691., Pan et al. 2011Pan M., Pierce G.J., Cunningham C.O., et al. 2011. Seasonal and interannual variation of decapod larval abundance from two coastal locations in Scotland, UK. J. Mar. Biol. Assoc. UK 91: 1443-1451.). However, comparatively little is known about the seasonality of decapod larvae in tropical and subtropical regions (Epifanio and Dittel 1984Epifanio C.E., Dittel A.I. 1984. Seasonal abundance of brachyuran crab larvae in a tropical estuary: Gulf of Nicoya, Costa Rica, Central América. Estuaries 7: 501-505., Reyns and Sponaugle 1999Reyns N., Sponaugle S. 1999. Patterns and processes of brachyuran crab settlement to Caribbean coral reefs. Mar. Ecol. Prog. Ser. 185: 155-170.). It is expected that the higher and more stable temperature throughout the year in lower latitudes favours continuous reproduction (Bauer 1992Bauer R.T. 1992. Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. Invertebr. Reprod. Dev. 3: 193-202.), leading to a weaker seasonality of decapod larvae in the plankton.

In the subtropical waters of the Canary Islands, decapod crustacean fauna is relatively well studied. Currently, around 300 species have been reported (González and Quiles 2003González J.A., Quiles J.A. 2003. Orden Decapoda. In: Moro L., Martín J.L., et al. (eds). Lista de especies marinas de Canarias (algas, hongos, plantas y animales). Consejería de Política Territorial y Medio Ambiente del Gobierno de Canarias. pp. 248., Moro et al. 2014Moro L., Herrera R., Ortea J., et al. 2014. Aportaciones al conocimiento y distribución de los decápodos y estomatópodos (Crustacea: Malacostraca) de las islas Canarias. Rev. Acad. Canar. Cienc. 26: 33-82., González 2016González J.A. 2016. Brachyuran crabs (Crustacea: Decapoda) from the Canary Islands (eastern Atlantic): checklist, zoogeographic considerations, and conservation. Sci. Mar. 80: 89-102.), yet knowledge of distribution, population dynamics and reproductive biology is limited to a few key species found in seagrass meadow ecosystems (García-Sanz et al. 2014García-Sanz S., Navarro P.G., Landeira J.M., et al. 2014. Colonization patterns of decapods into artificial collectors: seasonality between habitat patches. J. Crustac. Biol. 34: 431-441.) and to some deep-water species with commercial interest for small-scale local fisheries (Tuset et al. 2009Tuset V.M., Pérez-Peñalvo J.A., Delgado J., et al. 2009. Biology of the deep-water shrimp Heterocarpus ensifer (Caridea: Pandalidae) off the Canary, Madeira and the Azores islands (Northeastern Atlantic). J. Crustac. Biol. 2: 507-515., González et al. 2016aGonzález J.A., Pajuelo J.G., Triay-Portella R., et al. 2016a. Latitudinal patterns in the life-history traits of three isolated Atlantic populations of the deep-water shrimp Plesionika edwardsii (Decapoda, Pandalidae). Deep-Sea Res. I 117: 28-38., Triay-Portella et al. 2017Triay-Portella R., Ruiz-Díaz R., Pajuelo J.G., et al. 2017. Ovarian maturity, egg development, and offspring generation of the deep-water shrimp Plesionika edwardsii (Decapoda, Pandalidae) from three isolated populations in the eastern North Atlantic. Mar. Biol. Res. 13: 174-187.). Similarly, little is known about the larval biology of decapods in the area, although significant efforts have recently been focused on the larval development of species whose larval morphology is still unknown (e.g. Landeira and Cuesta 2012Landeira J.M., Cuesta J.A. 2012. Morphology of the second zoeal stage of Grapsus adscensionis (Osbeck, 1765) (Crustacea, Decapoda, Grapsoidea) confirms larval characters of the family Grapsidae. Zootaxa 64: 59-64., Landeira et al. 2014Landeira J.M., Jiang G.-C., Chan T.-Y., et al. 2014. Description of the decapodid stage of Plesionika narval (Fabricius, 1787) (Decapoda: Caridea: Pandalidae) identified by DNA barcoding. J. Crustac. Biol. 34: 377-387., 2015Landeira J.M., Jiang G.-C., Chan T.-Y., et al. 2015. Redescription of the early larval stages of the pandalid shrimp Chlorotocus crassicornis (Decapoda: Caridea: Pandalidae). Zootaxa 4013: 100-110.). Accurate taxonomic descriptions have aided the identification of larvae in the plankton and the study of transport processes in the Canary-African Coastal Transition Zone. The spatial distribution of larvae over the shelf of the island of Gran Canaria shows a clear pattern, in which larval abundances are much higher in the weak flow area around the stagnation point upstream of the island and the warm lee region downstream, where less intense winds occur (Landeira et al. 2009Landeira J.M., Lozano-Soldevilla F., Hernández-León S., et al. 2009. Horizontal distribution of invertebrate larvae around the oceanic island of Gran Canaria: the effect of mesoscale variability. Sci. Mar. 73: 761-771., 2013Landeira J.M., Lozano-Soldevilla F., Hernández-León S. 2013. Temporal and alongshore distribution of decapod larvae in the oceanic island of Gran Canaria (NW Africa). J. Plankton Res. 35: 309-322.). In open waters, the larval abundance is usually very low, but there is a clear physical/biological coupling between mesoscale oceanographic activity and decapod larvae distribution. Eddies generated downstream of the archipelago when the Canary Current impinges upon the island topography (Hernández-Guerra et al. 1993Hernández-Guerra A., Arístegui J., Cantón M., et al. 1993. Phytoplankton pigment patterns in the Canary Islands as determined using Coastal Zone Colour Scanner data. Int. J. Remote Sens. 14: 1431-1437., Sangrà et al. 2007Sangrà P., Auladell M., Marrero-Díaz A., et al. 2007. On the nature of oceanic eddies shed by the Island of Gran Canaria. Deep-Sea Res. I 54: 687-709.) act as oceanic retention zones for larvae of neritic species (Landeira et al. 2010Landeira J.M., Lozano-Soldevilla F., Hernández-León S., et al. 2010. Spatial variability of planktonic invertebrate larvae in the Canary Islands area. J. Mar. Biol. Assoc. UK 90: 1217-1225., 2012Landeira J.M., Lozano-Soldevilla F., Barton E.D. 2012. Mesoscale advection of Upogebia pusilla larvae through an upwelling filament in the Canaries Coastal Transition Zone (CTZ). Helgol. Mar. Res. 66: 537-544., 2017Landeira J.M., Brochier T., Mason E., et al. 2017. Transport pathways of decapod larvae under intense mesoscale activity in the Canary-African Coastal Transition Zone: implications for population connectivity. Sci. Mar. 81: 299-315.). Furthermore, it has been observed that filaments of upwelled waters originating over the continental shelf transport larvae from the African coast towards the ocean, indicating that they provide a conduit to the islands that connects populations (Brochier et al. 2011Brochier T., Mason E., Moyano M., et al. 2011. Ichthyoplankton transport from the African coast to the Canary Islands. J. Mar. Syst. 89: 109-122., Landeira et al. 2012Landeira J.M., Lozano-Soldevilla F., Barton E.D. 2012. Mesoscale advection of Upogebia pusilla larvae through an upwelling filament in the Canaries Coastal Transition Zone (CTZ). Helgol. Mar. Res. 66: 537-544., 2017Landeira J.M., Brochier T., Mason E., et al. 2017. Transport pathways of decapod larvae under intense mesoscale activity in the Canary-African Coastal Transition Zone: implications for population connectivity. Sci. Mar. 81: 299-315.).

In the context of climate change, several studies have described pronounced responses by marine ecosystems to global warming. Currently, a shift of the biogeographical distribution and phenological patterns is being observed in response to increasing temperature trends (Parmesan 2006Parmesan C. 2006. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37: 637-669.). In the North Sea, long-term time series from continuous plankton recorders have revealed earlier temporal occurrences of several species of crustacean decapods (Lindley et al. 1993Lindley J.A., Williams R., Hunt H.G. 1993. Anomalous seasonal cycles of decapod crustacean larvae in the North Sea plankton in an abnormally warm year. J. Exp. Mar. Biol. Ecol. 172: 47–65.), increased abundances of decapod larvae (Kirby et al. 2008Kirby R., Beaugrand G., Lindley J.A. 2008. Climate-induced effects on the meroplankton and the benthic-pelagic ecology of the North Sea. Limnol. Oceanogr. 53: 1805-1815., Kirby and Beaugrand 2009Kirby R.R., Beaugrand G. 2009. Trophic amplification of climate warming. Proc. R. Soc. Lond. Ser. B Biol. Sci. 276: 4095-4103.) and increasing spatial extents of warm-water species, as well as the arrival of new species (Lindley et al. 2010Lindley J.A., Beaugrand G., Luczak C., et al. 2010. Warm-water decapods and the trophic amplification of climate in the North Sea. Biol. Lett. 6: 773-776.). At lower latitudes, the effects of this warming are expected to include increased disturbances in crustacean decapods dynamics, but with as yet unknown consequences. It is therefore important to study the current state of decapod larvae assemblages in order to predict and/or detect changes in their population dynamics due to a future warming scenario in the tropics and subtropics. For this reason, using an intensive sampling monitoring off Gran Canaria, we describe here for the first time the seasonal assemblage of the decapod larvae community and associated environmental variables at the Canary Islands. Our primary aim was to test whether the larval community in the subtropical waters of the Canary Islands shows a lesser seasonality than that at other northern latitudes in the eastern Atlantic. Moreover, we report the first record of several species based on the presence of their larval stages in plankton samples.

MATERIALS AND METHODSTop

Sampling and laboratory analysis

In the framework of the ConAfrica project, weekly sampling was carried out from January 2005 to December 2006 (n=76 samples) during daylight hours aboard the R/V Solana II. This study focuses on station 1 (28°04.00'N 15°21.62'W), located over the 100 m isobath in an area of weak flow associated with the stagnation point upstream of the island (Moyano and Hernández-León 2011Moyano M., Hernández-León S. 2011. Intra- and interannual variability in the larval fish assemblage off Gran Canaria (Canary Islands) over 2005–2007. Mar. Biol. 158: 257-273., Landeira et al. 2013Landeira J.M., Lozano-Soldevilla F., Hernández-León S. 2013. Temporal and alongshore distribution of decapod larvae in the oceanic island of Gran Canaria (NW Africa). J. Plankton Res. 35: 309-322., Fig. 1). Zooplankton were collected using a Bongo net of 40 cm mouth diameter fitted with nets of 200 µm mesh size. The net was towed obliquely from 90 m to the surface at 2 knots (⁓1 m s–1) and a wire speed of 0.5 m s–1, and it was attempted to maintain a wire angle of approximately 45°. Flow rate was estimated using calibrated flowmeters (General Oceanics), and the mean volume of water filtered was 27.84 m3. For taxonomic identification, one of the samples was immediately fixed in a 4% solution of formalin in seawater. Prior to zooplankton sampling, vertical profiles of temperature, salinity and fluorescence were recorded using a CTD SBE25 (Sea-Bird Electronics, Inc., Bellevue, WA, USA). Phytoplankton chlorophyll a was derived from water samples taken in the mixed layer at a depth of 15 m with a Niskin bottle.

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Fig. 1. – Study area in the NE Atlantic, showing the location of the sampling station (black triangle) near the island of Gran Canaria.

In the laboratory, decapod larvae were sorted and quantified. For holoplanktonic pelagic shrimps which are planktonic during their whole lives (e.g. Lucifer typus), only larval stages were analysed. Following Anger (2001)Anger K. 2001. The Biology of Decapod Crustacean Larvae. Crustacean Issues: 14. A.A. Balkema Publishers. and Martin et al. (2014)Martin J.W., Olesen J., Høeg J.T. 2014. Atlas of Crustacean Larvae. John Hopkins Univ. Press., the transition from planktonic to benthic stages such as the decapodite stage in Caridea or megalopae in Brachyura were considered as last larval stages, whereas postlarval stages were not considered in this study. Larvae were identified using the guides given by dos Santos and Lindley (2001)Dos Santos A., Lindley J.A. 2001. Crustacea Decapada: Larvae. II Dendrobranchiata. (Aristeidae, Benthesicymidae, Penaeidae, Solenoceridae, Sicyonidae, Sergestidae and Luciferidae). ICES Identif. Leafl. Plankton 186. and dos Santos and González-Gordillo (2004)Dos Santos A., González-Gordillo J.I. 2004. Illustrated key for the identification of the Pleocyemata (Crustacea: Decapoda) zoeal stages, from the coastal region of south-western Europe. J. Mar. Biol. Assoc. U.K. 84: 205-227., and using the specific taxonomic descriptions recommended in the checklist of González-Gordillo et al. (2001)González-Gordillo J.I., dos Santos A., Rodríguez A. 2001. Checklist and annotated bibliography of decapod crustacean larvae from the Southwestern European coast (Gibraltar Strait area). Sci. Mar. 65: 275-305. General taxonomical nomenclature follows De Grave et al. (2009)De Grave S., Pentcheff N.D., Ahyong S.T. et al. 2009. A classification of living and fossil genera of decapod crustaceans. Raff. Bull. Zool. 21: 1-109.. The catches were standardized by number of decapod larvae per 100 m3.

Data analysis

The Shannon–Wiener diversity index (H'),

H = i=1 S p i ln p i

(where S is the number of species and pi is the proportion of individuals in species i), was used to analyse changes in temporal and spatial diversity in the decapod larvae community. The parametric statistical method (Student t test, p>0.05) was used to evaluate interannual differences in larval abundance and diversity (previously tested for homogeneity of variances using Levene’s test). Multivariate analysis was used to identify larval assemblages with distinct community structure. Only species present in both 2005 and 2006 were used in the analysis in order to eliminate the effect of rare and multispecies groups (e.g. Sergestidae spp., Pagurus spp.). A total of 49 species were left from the initial 105.

In a first step, to examine temporal differences between months, within years and between years, an analysis of similarities (two-way nested ANOSIM) was performed on the species resemblance matrix using the log-transformed abundance data from all the samples in a Bray-Curtis similarity matrix. After this analysis, using the same Bray-Curtis similarity matrix, a non-metric multidimensional scaling (MDS) was performed to obtain a graphical ordination of the samples (Clarke and Warwick 2001Clarke K., Warwick R. 2001. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. 2nd edition: PRIMER-E, Plymouth.). It was assumed that stress coefficients greater than 0.15 indicate a good representation of data (Clarke and Gorley 2006Clarke K., Gorley R. 2006. PRIMER v6: user manual/tutorial. PRIMER-E Ltd., Plymouth.).

Due to the absence of any temporal structure in the decapod larvae community (see Results), forced by the elevated number of taxa and the weak seasonality of decapod larvae in subtropical waters (Reyns and Sponaugle 1999Reyns N., Sponaugle S. 1999. Patterns and processes of brachyuran crab settlement to Caribbean coral reefs. Mar. Ecol. Prog. Ser. 185: 155-170.), a month-averaged larval abundance data was used in a second step of the analysis (removing the factor year). In this second step, in order to divide the 12 months into distinct periods of larval assemblages, a cluster analysis and similarity profile routine (SIMPROF; p<0.01; 999 permutations) were performed using the log-transformed abundance data in a Bray-Curtis similarity matrix. SIMPROF is a permutation test that objectively determines whether any significant group structure exists within a set of samples (Clarke and Gorley 2006Clarke K., Gorley R. 2006. PRIMER v6: user manual/tutorial. PRIMER-E Ltd., Plymouth.).

After this analysis, using the same Bray-Curtis similarity matrix, a non-metric MDS was performed. The significant results of the SIMPROF test were entered into the MDS plot to assess the level of agreement between the two techniques. Complementarily, the RELATE procedure, employing Spearman rank correlation coefficients (p), was used to determine whether the series of sequential points for mean monthly samples on MDS ordination plots approximated a circle and, if so, the extent to which the distribution of those points was correlated with a true circle (Clarke and Warwick 2001Clarke K., Warwick R. 2001. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. 2nd edition: PRIMER-E, Plymouth.). The groups of months detected were used as factors to test significant differences in temporal larval assemblages of decapod species using a one-way similarity analysis (ANOSIM).

A similarity percentages (SIMPER) test was then used to determine which species contributed most to characterization of each period of distinct larval assemblage (Clarke and Warwick 2001Clarke K., Warwick R. 2001. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. 2nd edition: PRIMER-E, Plymouth., Clarke and Gorley 2006Clarke K., Gorley R. 2006. PRIMER v6: user manual/tutorial. PRIMER-E Ltd., Plymouth.). The non-parametric Spearman rank correlation was used to explore the relationship between sea surface temperature, salinity and chlorophyll a, and decapod larvae variables (total abundance and diversity). Finally, an MDS plot was represented by superimposing bubbles of increasing size related to significantly correlated variables in order to visualize the link with larval assemblages. Statistical analyses were carried out using PRIMER v.6.1 and SPSS 15.0.

RESULTSTop

Hydrographic conditions

Temperature showed a consistent seasonal trend in which the heating due to strong insolation led to maximum values in the mixed layer at 20-30 m (22.9°C in 2005 and 24.1°C in 2006) from August to October. The cooling of the water column started in November and finished around March-April, showing minimum values of 17.7°C in 2015 and 18.3°C in 2016 (Fig. 2). Salinity did not show a seasonal pattern and ranged from 36.54 to 36.97 (Fig. 2). The temporal distribution of chlorophyll a was negatively correlated with temperature (Spearman rank correlation: r=–0.73, p<0.01) and showed the typical seasonality of the Canary Island waters (Table 1, Fig. 2). The quasi-permanent thermocline, which promotes oligotrophic conditions during most of the year and limits phytoplankton production in the Canary Islands (Arístegui et al. 2001Arístegui J., Hernández-León S., Montero M.F., et al. 2001. The seasonal planktonic cycle in coastal waters of the Canary Islands. Sci. Mar. 65: 51-58.), led to standing stocks of chlorophyll a lower than 0.2 mg m–3 during the summer (Fig. 2). This situation changed in winter, when the temperature droped below 19°C and the cooling of the surface eroded the thermocline, promoting the development of a najor phytoplankton bloom in February-March, followed by another smaller peak around April known as the late winter bloom. Interannual differences were observed. The highest chlorophyll a values (0.9 mg m–3) occurred during the bloom of 2005, with a mean standing stock of 0.7±0.16 mg m–3. In 2006 the peak occurred during the same period but was weaker, with a mean standing stock of 0.36±0.05 mg m–3 and maximum values of 0.47 mg m–3. The temporal evolution of temperature suggested different durations of the mixing period. In January 2006 the temperature was still above 19°C, preventing deep convection. In May the heating of the surface waters was already visible, especially in 2006, when the temperature was above 20°C at the beginning of the month. This situation led to a shorter mixing period in 2006 that promoted a lesser phytoplankton bloom.

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Fig. 2. – Temporal distribution of temperature (°C), salinity (practical salinity unit, PSU) at 2 m depth, and average chlorophyll a (15-75 m) (mg Chl-a m–3) from January 2005 to December 2006. Vertical profiles of temperature, salinity and chlorophyll a are averaged values for January, May and October.

Table 1. – Matrix showing the Spearman correlation coefficients for decapod larvae variables (abundance, nº larvae/100 m3; diversity, Shannon diversity index values) and environmental variables (temperature, °C; salinity; chlorophyll a, mg Chl-a m–3) at the surface (2 m depth); * p<0.05; ** p<0.01.

Abundance Diversity Temperature Salinity
Abundance
Diversity 0.84**
Temperature 0.43** 0.33**
Salinity 0.25 0.12 0.37**
Chlorophyll a –0.27* –0.24** –0.73** –0.41**

Decapod larvae community

A total of 6967 larvae belonging to 105 different taxa were identified during the two-year study. Gathered in different suborders, the Pleocyemata and Dendrobranchiata were represented by 85 and 20 taxa, respectively. Within the Pleocyemata, the infraorders with the highest number of taxa were Brachyura (36 taxa) and Caridea (31 taxa). Average species diversity was relatively high (2.40±0.59), with the highest values (>3) in June-August of both years and the lowest (0.60) in January 2005 (Fig. 3). A significant positive correlation with temperature (Spearman rank correlation: r=0.33, p<0.01) was also evidenced this tendency (Table 1). Differences in diversity between years were also significant (Student t test, df=74, t=–2.982, p=0.004), with 2005 showing a lower mean value (2.19±0.86) than 2006 (2.57±0.44).

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Fig. 3. – Temporal variation of the abundance (larvae/100 m3) (a) and Shannon–Wiener diversity index (H’) (b) of decapod larvae. Boxplots show yearly comparisons of abundance (c) and diversity (d). In each boxplot, the median (solid line) is indicated in the centre of the box and the edges of the box are the 25th and 75th percentiles; whiskers extend to the most extreme data points that were not considered to be outliers. Results from the Student t test are highlighted as follow: * p<0.05, ** p<0.01.

In terms of relative abundance, the infraorders Anomura and Caridea accounted for 33.4% and 32.8% of the total decapod larvae catches, respectively. Other less abundant taxonomic groups were Brachyura (17.5%), Dendrobranchiata (17.5%), Axiidea and Gebiidea (6%). Achelata and Stenopodidea did not show abundance greater than 5%, while Polychelida, Astacidea, and Glypheidea (this infraorder has not been recorded in the Canary Islands) were not observed in the samples (Table 2). The remaining infraorders are not present in the Canary Islands. The most abundant families within Anomura were Galatheidae (12.2%), Diogenidae (9.2%), and Paguridae (11.8%) due to the main contribution of Galathea intermedia, Calcinus tubularis and Pagurus spp. (Table 2). In Caridea, the families Apheidae, Hippolytidae and Processidae had abundances of around 7% of the total sample, with Processa nouveli and Latreutes fucorum as the most abundant species. The families Brachyura, Majidae, Xanthidae and Grapsidae accounted for around 3% of total abundance. The average abundances of Upogebia spp. (3.8%) and Pandalina brevirostris (3.1%) were also noteworthy. Regarding adult habitat, larvae of benthic species (86.1%) were more abundant than larvae of pelagic species (13.9%) (Table 2). Larvae in the first stage of development, zoea I, accounted for 37.8±13.4% of the total decapod larvae, whereas larvae in the last stage of development always accounted for less than 5% of the total larvae.

Table 2. – Taxonomic list of decapod larvae collected in Gran Canaria, showing the monthly presence/absence.

J F M A M JN JL A S O N D
DENDROBRANCHIATA
Benthesicymus sp. X X
Gennadas sp. X X X X X X X X X
Parapenaeus longirostris (Lucas, 1846) X X X X
Funchalia spp. X
Solenocera membranacea (Risso, 1816) X
Lucifer typus H. Milne-Edwards, 1837 X X X X X X X X X X X X
Petalidium spp. X X X
Allosergestes pectinatus (Sund, 1920) X X X X X X X X X X X
Allosergestes sargassi (Ortmann, 1893) X X X X X
Deosergestes curvatus (Crosnier & Forest, 1973) X X X X X X
Deosergestes henseni (Ortmann, 1893) X X X X X X
Parasergestes armatus (Krøyer, 1855) X
Parasergestes diapontius (Bate, 1881) X X X X
Parasergestes vigilax (Stimpson, 1860) X X X X X X X X X
Sergestes atlanticus Milne-Edwards, 1830 X X X X X X X X X
Sergestes cornutus Krøyer, 1855 X X X X X
Sergia robusta (Smith, 1882) X X X X X X X X X X
Sergia splendens (Sund, 1920) X X X X X X X
Sergia tenuiremis (Krøyer, 1855) X
Sergestidae spp. X X X X
PLEOCYEMATA
CARIDEA
Acanthephyra spp. X X X X X X
Oplophoridae spp. X X X X
Nematocarcinus spp. X X X
Cinetorhynchus rigens (Gordon, 1936) X X X X X X X X
Brachycarpus biunguiculatus (Lucas, 1846) X X X X X
Pontonia pinnophylax (Otto, 1821) X
Pontonia spp. X X X X X X
Periclimenes sp. X X X X X X X X X X X X
Athanas nitescens (Leach, 1813) X X X X X X X X X
Alpheus glaber (Olivi, 1792) X X X X X X X X X X
Alpheus macrocheles (Hailstone, 1835) X X X X X X X X X X
Alpheus spp. X X X X X X X
Alpheidae spp. X X X X X X X
Eualus occultus (Lebour, 1936) X X X X X X X X X X
Eualus pusiolus (Krøyer, 1841) X
Hippolyte sp. X X X X X X X X
Latreutes fucorum (Fabricius, 1798) X X X X X X X X X X X X
Lysmata seticaudata (Risso, 1816) X X X X X X X X X
Lysmata sp. X X
Processa edulis (Risso, 1816) X X X X X X
Processa modica Williamson & Rochanaburanon, 1979 X X X X X X X X X X
Processa nouveli Al-Adhub & Williamson, 1975 X X X X X X X X X X X X
Processa spp. X X X X X X X X X
Pandalina brevirostris (Rathke, 1843) X X X X X X X X X X X
Pandalidae spp. X X X X X X X X X X X X
Aegaeon cataphractus (Olivi, 1792) X X X X
Philocheras bispinosus (Hailstone, 1835) X X X X X X X X
Philocheras sculptus (Bell, 1847) X X X X X X X X X X
Philocheras trispinosus (Hailstone. 1835) X
Crangon crangon (Linnaeus, 1758) X
AXIIDEA
Necallianassa truncata (Giard & Bonnier, 1890) X X X X X X X
Pestarella candida (Olivi, 1792) X
Callianasidae SL16 X X X X
GEBIIDEA
Upogebia sp. X X X X X X X X X X
STENOPODIDEA
Stenopus spinosus Risso, 1827 X
Stenopidae sp1. X
ACHELATA
Scyllarus spp. X X X X X X X X X X
ANOMURA
Galathea intermedia Lilljeborg, 1851 X X X X X X X X X X X X
Munida spp. X X X X X X X X X X X
Clibanarius aequabilis (Dana, 1851) X X X X X X X X X X X
Dardanus arrosor (Herbst, 1796) X X X X X X
Calcinus tubularis (Linnaeus, 1767) X X X X X X X X X X
Pagurus spp. X X X X X X X X X X X X
Nematopagurus longicornis A. Milne-Edwards & Bouvier, 1892 X X X X X X
Porcellana platycheles (Pennant, 1777) X
Albunea carabus (Linnaeus, 1758) X X
BRACHYURA
Dromia personata (Linnaeus, 1758) X
Ethusa mascarone (Linnaeus, 1758) X X
Ebalia tumefacta (Montagu, 1808) X X X X X X X X X X
Ebalia spp. X X X X X X
Ilia nucleus (Linnaeus, 1758) X X X X X X X X X X X X
Maja brachydactyla Balss, 1922 X X
Maja spp. X X X X
Acanthonyx lunulatus (Risso, 1816) X X X X
Pisa tetraodon (Pennant, 1777) X X X X X X X X X X X X
Stenorhynchus lanceolatus (Brullé, 1837) X X X X X
Inachus spp. X X X
Herbstia condyliata (Fabricius, 1787) X
Macropodia sp. X
Eurynome spp. X X X
Majidae spp. X X X X X X X X X X X
Xantho hydrophilus (Herbst, 1790) X X X X X X X X X
Xantho spp. X X X X X X X X X X X
Pilumnus spp. X
Monodaeus couchii (Couch, 1851) X X X
Nanocassiope melanodactyla (A. Milne-Edwards, 1867) X X X X X X X X X X X X
Liocarcinus spp. X X X X X X X X
Macropius spp. X
Atelecyclus spp. X X X X X X X X X X X
Parthenope spp. X X X X X X X X X X X X
Distolambrus maltzami (Miers, 1881) X X
Goneplax rhomboides (Linnaeus, 1758) X X X X X
Geryonidae spp. X X X X
Grapsus adscensionis (Osbeck, 1765) X X X X X X X X X
Pachygrapsus spp. X X X X X X X X X
Planes minutus (Linnaeus, 1758) X X
Percnon gibbesi (H. Milne-Edwards, 1853) X X X X X X X X X X X
Plagusia depressa (Fabricius, 1775) X X X X X X X X X X
Calappa granulata (Linnaeus, 1758) X X X X X X
Grapsidae spp. X X

Total abundances ranged from a minimum value of 30.2 larvae/100 m3 recorded in February 2005 to the maximum value of 2925 larvae/100 m3 in 12 August 2006. The mean abundance in 2005 (281.02±86.35 larvae/100 m3) was significantly lower (Student t test, df=74, t=–2.07, p=0.021) than in 2006 (478.14±116.13 larvae/100 m3). Decapod larvae were present in the plankton all year round, making it difficult to observe, a priori, any seasonal/interannual patterns (Fig. 3). A two-way ANOSIM test revealed a slight significant difference among months (Global R=0.372, p=0.03) but not among years (Global R=0.133, p=0.4). This result was supported by the MDS plot, which showed a poor spatial ordination of the samples based on their decapod larvae composition (Fig. 4).

figure4

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Fig. 4. – Non-metric multidimensional scaling ordination based on the Bray-Curtis similarity matrix of decapod larval abundance, using all samples collected in 2005 and 2006.

However, when the factor year was removed and month-averaged larval abundance data were used, the multivariate statistical analysis revealed seasonality in decapod larvae community (Fig. 5). Two significantly different groups of months (p<0.001) were distinguished using SIMPROF at a 58% level of similarity. An MDS plot (2D stress, 0.14) with a superimposed significant cluster shows the separation of the two distinct larval assemblages. A “warm” cluster includes May-September, while the other “cold” cluster includes November-April, and October appears as a transition between the two seasons (Fig. 5). In this ordination, the months tend to undergo a clockwise cyclical spatial distribution (Fig. 5), and RELATE confirmed that the cyclicity was consistent with that of a circle (p=0.001), with a rank correlation coefficient of 0.485. Moreover, the ANOSIM routine revealed that cold and warm larval assemblages were significantly different (Global R=0.489, p=0.002). The average abundance of decapod larvae, temperature, and chlorophyll a are superimposed as proportional bubbles over the MDS plot to visualize the relationship of these variables with the assemblages (Fig. 5), showing that during the warm period the larval abundance is also higher, in agreement with the positive correlation (Spearman rank correlation: r=0.43, p<0.01) between these two variables (Table 1). Conversely, as mention above, chlorophyll a was higher during colder months and therefore negatively correlated (Spearman rank correlation: r=–0.27, p<0.05) with decapod larva abundance.

figure5

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Fig. 5. – Dendrogram showing the classification of months from the Bray-Curtis similarity matrix of monthly averages of decapod larval abundance (A) Non-metric multidimensional scaling (MDS) ordination based on the same similarity matrix. (B) Average temperature, chlorophyll a, larval abundance and species diversity for each month is superimposed as proportional bubbles over the MDS plot (C-F). Dotted lines separate larval assemblages at the 58% similarity threshold.

This larval assemblage was difficult to visualize in the temporal distribution plot of abundant species, since they were collected in almost every single sampling event, indicating year-round spawning (Figs 6, 7). However, the SIMPER routine revealed that changes in composition and/or abundance were characteristic of the warm and cold assemblages (Table 3). Warm assemblages were found in species that spawn in summer, such as Calcinus tubularis larvae primarily collected in summer (54.1±23.8 larvae/100 m3) and Nanocassiope melanodactyla that was abundant during this period (19.4±11.2 larvae/100 m3) (Fig. 6). In the case of the pelagic species Deosergestes henseni, the larvae were collected exclusively in summer and showed a peak around June (19.9±8.8 larvae/100 m3), and Parasergestes vigilax was especially abundant during the summer and autumn of 2006 (Fig. 6). Pachygrapus spp. larvae showed a clear peak (May-October) in 2006 that was not evident in 2005. Other species, such as Alpheus glaber, Clibanarius aequabilis, Percnon gibbesi and Lysmata seticaudata, helped typify the warm assemblage but with lower (<4) similarity percentages (Fig. 6, Table 3). The cold assemblage was characterized by species that exhibited winter-autumn peaks, but their presence in the plankton was not always restricted to cold months. This is the case of Latreutes fucorum (peaks in late summer), and of Eualus occultus, Pandalina brevirostris, and Philocheras bispinosus (peaks in spring-summer) (Fig. 7). Other species that had elevated larval abundance throughout the year (e.g. Processa nouveli, Galathea intermedia, or Lucifer typus) contributed strongly to the cold assemblage but were also important for the warm assemblage (Table 3).

figure6

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Fig. 6. – Temporal distribution of decapod larval abundance (larvae/100 m3) of typical species of “warm assemblage” during the years 2005 and 2006. Temporal distribution of temperature (°C) at the surface (2 m depth) is also shown. Note that left y-axis scales differ among species.

figure7

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Fig. 7. – Temporal distribution of decapod larval abundance (larvae/100 m3) of typical species of “cold assemblage” during the years 2005 and 2006. Temporal distribution of temperature (°C) at the surface (2 m depth) is also shown. Note that left y-axis scales differ among species.

Table 3. – Values correspond to the percentage of similarity (SIMPER analysis) of the species that contributed to 80% of average similarity for each assemblage.

Cold
assemblage
Warm
assemblage
Processa nouveli 12.01 8.11
Galathea intermedia 9.52 9.37
Lucifer typus 7.84 4.56
Pandalina brevirostris 6.8 3.02
Latreutes fucorum 6.4 4.03
Pisa tetraodon 5.39 4.48
Alpheus macrocheles 5.26 2.98
Nanocassiope melanodactyla 4.39 8.44
Philocheras sculptus 4.52
Philocheras bispinosus 3.59
Eualus occultus 3.22
Allosergestes pectinatus 3.2
Xantho hydrophilus 3.16
Sergia robusta 3.08
Athanas nitescens 2.07
Calcinus tubularis 11.82
Alpheus glaber 4.63
Ebalia tumefacta 3.36
Deosergestes henseni 3.11
Clibanarius aequabilis 3.05
Percnon gibbesi 2.87
Lysmata seticaudata 2.22
Parasergestes vigilax 2.16
Necallianassa truncata 1.7

New records

We report, for the first time in the Canary Islands waters, the presence of larvae of the species Pandalina brevirostris, Processa edulis, Necallianasa truncata, Parapenaeus longirostris, Crangon crangon and Nematopagurus longicornis. All larval stages of P. brevirostris were found and, as mentioned above, it is an abundant species (mean abundance of 12.21 larvae/100 m3) characterizing the cold assemblage (Fig. 6, Table 3). Processa edulis (zoea I-III stages) was caught in March, May, June-September and November, when it peaked with a mean abundance of 10.18 larvae/100 m3 (Table 2). Larvae of mud shrimp N. truncata (zoea I-III stages) were frequently collected in the plankton, especially in summer, when they achieved significant concentrations in September (mean abundance of 44.46 larvae/100 m3). N. longicornis zoeae III and zoeae IV were observed in March (maximum value of 13.85 larvae/100 m3), July and December 2005 and in January and May 2006. P. longirostris larvae in protozoea III stage of development were observed sporadically in June (3.19 larvae/100 m3) and July (2.61 larvae/100 m3) 2005, and in February and December 2006 (around 7 larvae/100 m3). Only one larva (zoea IV) of C. crangon was caught in January 2006.

DISCUSSIONTop

Composition and larval assemblages

This description of the entire larval community of Gran Canaria provides valuable information about the composition and potential spawning season for the most abundant species, which have been largely under-studied. Broadly, the decapod larvae community in Gran Canaria is characterized by contracted larval hatching periods, significant contributions from pelagic species, and weaker seasonality in comparison with higher latitudes, but has two distinct larval assemblages.

The year-round occurrence of decapod larvae in the plankton indicates that crustacean decapods can reproduce throughout the year. The temporal distribution of decapod larvae suggests a contracted larval hatching period for many species, but with abundance peaks associated with seasonality. This characteristic pattern observed in the subtropical waters of Gran Canaria contrasts with what happens at higher latitudes of the NE Atlantic. For example, in Svalbard, in the Arctic Ocean, decapod larvae occurred in the plankton during short periods from May to August, with a peak in mid-June (Stübner et al. 2016Stübner E.I., Søreide J.E., Reigstad M., et al. 2016. Year-round meroplankton dynamics in high-Arctic Svalbard. J. Plankton Res. 38: 522-536.). In the North Sea, the presence of a marked seasonality characterized by the virtual absence of larvae from December to February and by the presence of two main abundance peaks in spring and summer and extending into autumn is well documented (Highfield et al. 2010Highfield J.M., Eloire D., Conway D.V.P., et al. 2010. Seasonal dynamics of meroplankton assemblages at station L4. J. Plankton Res. 32: 681-691., Pan et al. 2011Pan M., Pierce G.J., Cunningham C.O., et al. 2011. Seasonal and interannual variation of decapod larval abundance from two coastal locations in Scotland, UK. J. Mar. Biol. Assoc. UK 91: 1443-1451.). This larval seasonality is also visible, but the presence of larvae in the plankton is year-round at lower latitudes of the Mediterranean Sea (Bourdillon-Casanova 1960Bourdillon-Casanova L. 1960. Le méroplancton du Golfe de Marseille. Les larves de Crustacés Décapodes. Rec. Trav. Stat. Mar. d’Endoume 30: 1-286., Fusté 1982Fusté X. 1982. Ciclo anual de las larvas de Crustáceos Decápodos de la costa de Barcelona. Invest. Pesq. 46: 287-303.), the Atlantic coasts of Portugal (dos Santos 1999Dos Santos A. 1999. Larvas de crustáceos decápodes ao largo da costa portuguesa. PhD thesis. Universidade de Lisboa, Lisbon, Portugal, 278 pp.) and southern Spain (González-Gordillo and Rodríguez 2003). In temperate regions, increases in water temperature trigger breeding events in which reproduction intensifies. However, in the tropics and subtropics the higher and less variable temperatures favour continuous reproduction (Bauer 1992Bauer R.T. 1992. Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. Invertebr. Reprod. Dev. 3: 193-202.). For instance, xanthid larvae are found in the water column all year round at the Canary Islands, with settlement peaks in spring and autumn (García-Sanz et al. 2014García-Sanz S., Navarro P.G., Landeira J.M., et al. 2014. Colonization patterns of decapods into artificial collectors: seasonality between habitat patches. J. Crustac. Biol. 34: 431-441.), whereas in the southern Iberian Peninsula, xanthid larvae are only present in the plankton in spring (González-Gordillo and Rodríguez 2003González-Gordillo J.I., Rodríguez A. 2003. Comparative seasonal and spatial distribution of decapod larvae assemblages in three coastal zones off the south-western Iberian Peninsula. Acta Oecol. 24: S219-S233.), or from April to September (Paula 1987Paula J. 1987. Seasonal distribution of Crustacea Decapoda larvae in S. Torpes bay, South-western Portugal. Inves. Pesq. 51: 267-275.), with a restricted settlement period in July-October (Flores et al. 2002Flores A.A.V., Cruz J., Paula J. 2002. Temporal and spatial patterns of settlement of brachyuran crab megalopae at a rocky coast in central Portugal. Mar. Ecol. Prog. Ser. 229: 207-220.). The less variable annual temperature regime in the Canary Islands (18-24°C, Barton et al. 1998Barton E.D., Arístegui J., Tett P., et al. 1998. The transition zone of the Canary Current upwelling region. Prog. Oceanogr. 41: 455-504.) leads to a protracted breeding season coupled with multiple peaks of zoeae I, which may indicate non-synchronous release and the presence of multiple cohorts.

In addition, in coincidence with the results of Moyano and Hernández-León (2011)Moyano M., Hernández-León S. 2011. Intra- and interannual variability in the larval fish assemblage off Gran Canaria (Canary Islands) over 2005–2007. Mar. Biol. 158: 257-273. for fish larvae, we identified two distinct seasonal larval assemblages, “cold” and “warm”, in which temperature seemed to play a key role in structuring the temporal variability of the decapod larvae community. The cold assemblage (November-April) occurred during the mixing period, when low temperatures and surface cooling erode the thermocline, allowing diffusion of nutrients that promotes elevated production of phytoplankton and zooplankton (Arístegui et al. 2001Arístegui J., Hernández-León S., Montero M.F., et al. 2001. The seasonal planktonic cycle in coastal waters of the Canary Islands. Sci. Mar. 65: 51-58., Moyano and Hernández-León 2011Moyano M., Hernández-León S. 2011. Intra- and interannual variability in the larval fish assemblage off Gran Canaria (Canary Islands) over 2005–2007. Mar. Biol. 158: 257-273.). Species that were more abundant in winter-spring, such as P. nouveli, L. typus, Philocheras sculptus and G. intermedia, were typical of the cold assemblage. Little is known about their reproductive strategies, although results from settlement experiments conducted in seagrass meadows and macroalgal beds off Gran Canaria (García-Sanz et al. 2014García-Sanz S., Navarro P.G., Landeira J.M., et al. 2014. Colonization patterns of decapods into artificial collectors: seasonality between habitat patches. J. Crustac. Biol. 34: 431-441.) have provided valuable information that is in agreement with that observed in the present study, suggesting pelagic/benthic coupling. Thus, Galathea spp. (including G. intermedia) and Pagurus spp. had two settlement periods, but the main peak (April-May) is related to the highest larval abundance observed in the plankton in winter. During the warm assemblage period (May-September), the surface heating stratifies the water column. This leads to reformation of the main thermocline, which then limits vertical nutrient fluxes and phytoplankton production (Arístegui et al. 2001Arístegui J., Hernández-León S., Montero M.F., et al. 2001. The seasonal planktonic cycle in coastal waters of the Canary Islands. Sci. Mar. 65: 51-58., Moyano and Hernández-León 2011Moyano M., Hernández-León S. 2011. Intra- and interannual variability in the larval fish assemblage off Gran Canaria (Canary Islands) over 2005–2007. Mar. Biol. 158: 257-273.). High abundances of N. melanodactyla, D. henseni, C. tubularis and C. aequabilis are characteristic of this assemblage. The settlement of C. tubularis and grapsid crabs (including Pachygrapsus spp.) occurred from October to December (García-Sanz et al. 2014García-Sanz S., Navarro P.G., Landeira J.M., et al. 2014. Colonization patterns of decapods into artificial collectors: seasonality between habitat patches. J. Crustac. Biol. 34: 431-441.), just after the summer plankton peak. Larval abundance in summer of the pelagic shrimp D. henseni is also characteristic of this assemblage. This species is one of the most abundant of the mesopelagic community in Canary Island waters (Ariza et at. 2015Ariza V., Garijo J.C., Landeira J.M., et al. 2015. Migrant biomass and respiratory carbon flux by zooplankton and micronekton in the north east Atlantic Ocean (Canary Islands). Prog. Oceanogr. 134: 330-342.), although its larval stages have also been collected in September (FAX99 cruise, Landeira et al. 2017Landeira J.M., Brochier T., Mason E., et al. 2017. Transport pathways of decapod larvae under intense mesoscale activity in the Canary-African Coastal Transition Zone: implications for population connectivity. Sci. Mar. 81: 299-315.), and October-November (CANARIAS 9110 cruise, Landeira et al. 2009Landeira J.M., Lozano-Soldevilla F., Hernández-León S., et al. 2009. Horizontal distribution of invertebrate larvae around the oceanic island of Gran Canaria: the effect of mesoscale variability. Sci. Mar. 73: 761-771.), suggesting a longer spawning season than that observed in the present study.

The contribution of pelagic shrimps to the larval community is significantly higher than that reported from other Atlantic regions (e.g. from Portugal by dos Santos 1999Dos Santos A. 1999. Larvas de crustáceos decápodes ao largo da costa portuguesa. PhD thesis. Universidade de Lisboa, Lisbon, Portugal, 278 pp. and from southern Spain by González-Gordillo and Rodríguez 2003González-Gordillo J.I., Rodríguez A. 2003. Comparative seasonal and spatial distribution of decapod larvae assemblages in three coastal zones off the south-western Iberian Peninsula. Acta Oecol. 24: S219-S233.), indicating considerable oceanic influence on the coastal region of the Canary Islands (Arístegui et al. 2001Arístegui J., Hernández-León S., Montero M.F., et al. 2001. The seasonal planktonic cycle in coastal waters of the Canary Islands. Sci. Mar. 65: 51-58.). It seems that this is a common pattern, since relatively high larval densities of pelagic species over the island shelf have been reported in other archipelagos, such as the Balearic Islands in the western Mediterranean (Torres et al. 2014Torres A.P., dos Santos A., Balbín R., et al. 2014. Decapod crustacean larval communities in the Balearic Sea (western Mediterranean): seasonal composition, horizontal and vertical distribution patterns. J. Mar. Syst. 138: 112-126.) and Saint Paul’s Rock in the equatorial Atlantic (Brandão et al. 2012Brandão M.C., Koettker A.G., Freire A.S. 2012. Abundance and composition of decapod larvae at Saint Paul’s Rocks (equatorial Atlantic). Mar. Ecol. 34: 171-185.).

Several deep-water shrimp pandalids, particularly Plesionika narval (Fabricius, 1787) but also P. edwardsii (Brandt, 1851) and Heterocarpus ensifer A. Milne-Edwards, 1881, are targeted by local small-scale fisheries operating with bottom traps at some island localities (González 1995González J.A. 1995. Catálogo de los Crustáceos Decápodos de las Islas Canarias. Monografías del Instituto Canario de Ciencias Marina 1, ULPGC, Santa Cruz de Tenerife, Spain. pp 1-282.). Ovigerous females occur year-round but a mass spawning peak occurs in the Canary Islands in spring and summer (Tuset et al. 2009Tuset V.M., Pérez-Peñalvo J.A., Delgado J., et al. 2009. Biology of the deep-water shrimp Heterocarpus ensifer (Caridea: Pandalidae) off the Canary, Madeira and the Azores islands (Northeastern Atlantic). J. Crustac. Biol. 2: 507-515., González et al. 2016aGonzález J.A., Pajuelo J.G., Triay-Portella R., et al. 2016a. Latitudinal patterns in the life-history traits of three isolated Atlantic populations of the deep-water shrimp Plesionika edwardsii (Decapoda, Pandalidae). Deep-Sea Res. I 117: 28-38., Triay-Portella et al. 2017Triay-Portella R., Ruiz-Díaz R., Pajuelo J.G., et al. 2017. Ovarian maturity, egg development, and offspring generation of the deep-water shrimp Plesionika edwardsii (Decapoda, Pandalidae) from three isolated populations in the eastern North Atlantic. Mar. Biol. Res. 13: 174-187.). In the present study, larvae of Heterocarpus spp. and Plesionika spp. were included in Pandalidae spp., because it is still impossible to distinguish these two genera using morphological characters in view of their remarkable similarity. Despite this limitation, larvae of Pandalidae spp. were present in the plankton throughout the year and peaked in September, supporting the spawning period reported.

According to González (2016)González J.A. 2016. Brachyuran crabs (Crustacea: Decapoda) from the Canary Islands (eastern Atlantic): checklist, zoogeographic considerations, and conservation. Sci. Mar. 80: 89-102., intertidal crab species such as Plagusia depressa, Xantho spp., Grapsus adscensionis, Pachygrapsus spp. and Percnon gibbesi are intensively harvested, mainly by hand, to be used for human consumption and/or as bait by small-scale fisheries. Harvesting pressure is frequently high and, in some regions, there are clear symptoms of overexploitation. This author recommended an urgent study of basic biological parameters such as population status for the implementation of conservation measures (González 2016González J.A. 2016. Brachyuran crabs (Crustacea: Decapoda) from the Canary Islands (eastern Atlantic): checklist, zoogeographic considerations, and conservation. Sci. Mar. 80: 89-102.). The presence of these larvae in the plankton can be interpreted as an indicator of the breeding season of these species. Abundance of P. depressa and Pachygrapsus spp. peaked during summer, whereas P. gibbesi and G. adscensionis seem to have two peaks, in spring and summer, respectively.

Equally notable in our results is the absence of larvae from taxa that are common in our sampling region as adults. This was the case of the shrimp Palaemon elegans Rathke, 1837 and the crab Eriphia verrucosa (Forskål, 1775), which inhabit intertidal ponds and shallow water rocky shores (González 1995González J.A. 1995. Catálogo de los Crustáceos Decápodos de las Islas Canarias. Monografías del Instituto Canario de Ciencias Marina 1, ULPGC, Santa Cruz de Tenerife, Spain. pp 1-282., d’Udekem d’Acoz 1999D’Udekem d’Acoz C. 1999. Inventaire et distribution des crustacés décapodes de l’Atlantique nord-oriental, de la Méditerranée et des eaux continentales adjacentes au nord de 25°N. Belgique. Patrimoines naturels (MNHN/SPN) 40: 1-383.). The fact that we did not find these taxa is difficult to explain with the available data.

New records

Plankton surveys have proved useful for the assessment of diversity in marine ecosystems. This brings us the possibility of sampling, at the same time, larvae of both pelagic and benthic species inhabiting shallow, deep-water and/or cryptic habitats, which are sometimes difficult to collect as adults. For example, similar samplings have facilitated the detection of non-indigenous species such as a new unreported pinnotherid crab in the Gulf of Cádiz (Marco-Herrero et al. 2017Marco-Herrero E., Drake P., Cuesta J.A. 2017. Larval morphology and DNA barcodes as valuable tools in early detection of marine invaders: a new pea crab found in European waters. J. Mar. Biol. Assoc. UK 1-9. ). In the western Mediterranean Sea, the study of plankton samples has also led to the detection of larvae of the invasive shrimp Palaemon macrodactylus Rathbun, 1902 (Torres et al. 2012Torres A.P., dos Santos A., Cuesta J.A., et al. 2012. First record of Palaemon macrodactylus Rathbun, 1902 (Decapoda, Palaemonidae) in the western Mediterranean. Mediterr. Mar. Sci. 13: 278-282.), but it also has provided valuable information on deep-water species of interest for conservation and fishing exploitation, such as Aristeus antennatus (Risso, 1816), Parapenaeus longirostris and Scyllarides latus (Latreille, 1803) (Torres et al. 2013Torres A.P., dos Santos A., Alemany F., et al. 2013. Larval stages of crustacean species of interest for conservation and fishing exploitation in the western Mediterranean. Sci. Mar. 77: 149-160.).

In the present study, we identified larvae of species that have not yet been reported from the Canary Islands. For example, the high abundance and temporally stable occurrence of P. brevirostris, P. edulis, and N. truncata larvae suggest that these species may not only be present in the study region, but also relatively common. If the presence of adult populations is confirmed, the geographical distribution of these four species would extend to the south (d’Udekem D’Acoz 1999D’Udekem d’Acoz C. 1999. Inventaire et distribution des crustacés décapodes de l’Atlantique nord-oriental, de la Méditerranée et des eaux continentales adjacentes au nord de 25°N. Belgique. Patrimoines naturels (MNHN/SPN) 40: 1-383.).

We also report the occurrence of larval forms of unknown crustacean adults. This is the case of Stenopidae sp1 that were collected in November 2006. In the Canary Islands, Stenopus spinosus was the only member of Stenopodidea until the recent record of Spongiocaris koehleri (Caullery, 1896) observed by González et al. (2016b)González J.A., Triay-Portella J.A., Santana J.I. 2016b. Southernmost record of Spongiocaris koehleri (Decapoda, Stenopodidea, Spongicolidae) off the Canary Islands. Crustaceana 89: 1233-1238.. However, S. koehleri larvae cannot be found in the plankton since they have direct development (Kemp 1910Kemp S.W. 1910. The Decapoda collected by the “Huxley” from the North Side of the Bay of Biscay in August, 1906. J. Mar. Biol. Assoc. UK 8: 407-420.). This finding suggests that another stenopodid species may be present in the Canary Islands. Another example is the larval form of Callianasidae SL16, which was relatively abundant from May to August. This larval form was described by dos Santos (1999)Dos Santos A. 1999. Larvas de crustáceos decápodes ao largo da costa portuguesa. PhD thesis. Universidade de Lisboa, Lisbon, Portugal, 278 pp. from plankton specimens collected south of Portugal in July. It has also been observed in the NW African upwelling, where it was transported towards the ocean during a strong filament event in August-September 1999 (Landeira et al. 2017Landeira J.M., Brochier T., Mason E., et al. 2017. Transport pathways of decapod larvae under intense mesoscale activity in the Canary-African Coastal Transition Zone: implications for population connectivity. Sci. Mar. 81: 299-315.). The only callianassid species reported for the Canary Islands are Pestarella tyrrhena (Petagna, 1792) (González and Quiles 2003González J.A., Quiles J.A. 2003. Orden Decapoda. In: Moro L., Martín J.L., et al. (eds). Lista de especies marinas de Canarias (algas, hongos, plantas y animales). Consejería de Política Territorial y Medio Ambiente del Gobierno de Canarias. pp. 248.) and Pestarella candida (Moro et al. 2014Moro L., Herrera R., Ortea J., et al. 2014. Aportaciones al conocimiento y distribución de los decápodos y estomatópodos (Crustacea: Malacostraca) de las islas Canarias. Rev. Acad. Canar. Cienc. 26: 33-82.), which are also present off NW Africa and Portugal (d’Udekem D’Acoz 1999D’Udekem d’Acoz C. 1999. Inventaire et distribution des crustacés décapodes de l’Atlantique nord-oriental, de la Méditerranée et des eaux continentales adjacentes au nord de 25°N. Belgique. Patrimoines naturels (MNHN/SPN) 40: 1-383.). However, their larval morphology is clearly different, since Callianasidae SL16 has spines on the entire ventral margin of carapace, and in the other two species the spines are present only on the anteroventral margin (for details see the original descriptions listed in González-Gordillo et al. 2001González-Gordillo J.I., dos Santos A., Rodríguez A. 2001. Checklist and annotated bibliography of decapod crustacean larvae from the Southwestern European coast (Gibraltar Strait area). Sci. Mar. 65: 275-305.). Therefore, it is reasonable to think that another callianasid species is present in the study area.

The hermit crab N. longicornis is distributed at a depth of 70-800 m along the NE Atlantic coast, including Madeira, the Azores, Morocco, and Cape Verde Islands (d’Udekem d’Acoz 1999D’Udekem d’Acoz C. 1999. Inventaire et distribution des crustacés décapodes de l’Atlantique nord-oriental, de la Méditerranée et des eaux continentales adjacentes au nord de 25°N. Belgique. Patrimoines naturels (MNHN/SPN) 40: 1-383., d’Udekem d’Acoz and Wirtz 2002D’Udekem d’Acoz C. Wirtz P. 2002. Observations on some interesting coastal Crustacea Decapoda from the Azores, with a key to the genus Eualus Thallwitz, 1892 in the Northeastern Atlantic and the Mediterranean. Arquip.: Life Earth Sci. 19: 67-84.). The Canary Islands is the only archipelago in the area without records, so it seems that González (1995)González J.A. 1995. Catálogo de los Crustáceos Decápodos de las Islas Canarias. Monografías del Instituto Canario de Ciencias Marina 1, ULPGC, Santa Cruz de Tenerife, Spain. pp 1-282. was right when he suggested that this species could also be present in the Canary Islands. Crangon crangon is widely distributed along the NE Atlantic coasts from the White Sea and Iceland down to Morocco, in the Baltic Sea, the Mediterranean Sea, and also the Black Sea (d’Udekem d’Acoz 1999D’Udekem d’Acoz C. 1999. Inventaire et distribution des crustacés décapodes de l’Atlantique nord-oriental, de la Méditerranée et des eaux continentales adjacentes au nord de 25°N. Belgique. Patrimoines naturels (MNHN/SPN) 40: 1-383.). If this species was present in the Canary Islands, it would constitute the southernmost population. However, in our opinion it is unlikely that find adult populations will be found there since there is no evidence for its occurrence in other northern Macaronesian archipelagos, such as the Selvagen Islands, Madeira and the Azores (d’Udekem d’Acoz 1999D’Udekem d’Acoz C. 1999. Inventaire et distribution des crustacés décapodes de l’Atlantique nord-oriental, de la Méditerranée et des eaux continentales adjacentes au nord de 25°N. Belgique. Patrimoines naturels (MNHN/SPN) 40: 1-383.). Moreover, C. crangon is an epibenthic shrimp that preferably inhabits soft-sediment in estuarine habitats (Holthuis 1980Holthuis L.B. 1980. FAO species catalogue. Vol. 1. Shrimps and prawns of the world. An annotated catalogue of species of interest to fisheries. FAO Fish. Synop. 125: 1-261.) that do not exist in the Canary Islands. It is possible that this larva reached the Gran Canaria coast transported by upwelling filaments from Africa, as has been suggested by Landeira et al. (2017)Landeira J.M., Brochier T., Mason E., et al. 2017. Transport pathways of decapod larvae under intense mesoscale activity in the Canary-African Coastal Transition Zone: implications for population connectivity. Sci. Mar. 81: 299-315., but with the available data it is not possible to support this hypothesis.

P. longirostris is one of the most important commercial shrimps found in the Mediterranean Sea and the NE Atlantic, from Galicia to Angola (d’Udekem d’Acoz 1999D’Udekem d’Acoz C. 1999. Inventaire et distribution des crustacés décapodes de l’Atlantique nord-oriental, de la Méditerranée et des eaux continentales adjacentes au nord de 25°N. Belgique. Patrimoines naturels (MNHN/SPN) 40: 1-383., Holthuis 1980Holthuis L.B. 1980. FAO species catalogue. Vol. 1. Shrimps and prawns of the world. An annotated catalogue of species of interest to fisheries. FAO Fish. Synop. 125: 1-261.). P. longirostris larvae have already been observed offshore, south of the Canary Islands in association with an African upwelling filament but, until now, these larvae have never been sampled over the island shelf (Landeira et al. 2009Landeira J.M., Lozano-Soldevilla F., Hernández-León S., et al. 2009. Horizontal distribution of invertebrate larvae around the oceanic island of Gran Canaria: the effect of mesoscale variability. Sci. Mar. 73: 761-771.). The presence of extensive adult populations is unlikely but the recent observations of single specimens of Penaeus kerathurus (Forskål, 1775) by different scuba divers in muddy-sandy habitats of Lanzarote, Gran Canaria and Tenerife islands (Moro et al. 2014Moro L., Herrera R., Ortea J., et al. 2014. Aportaciones al conocimiento y distribución de los decápodos y estomatópodos (Crustacea: Malacostraca) de las islas Canarias. Rev. Acad. Canar. Cienc. 26: 33-82.) make the occurrence of P. longirostris more probable in the Canary Islands.

Future prospects

This study provides accurate information about the composition and assemblage of decapod larvae in the Canary Islands region. Furthermore, the data collected during this study provide a baseline for future comparisons with respect to fishery pressure and climate variability. Despite the less evident seasonality displayed by most of the species examined, we identify two distinct temporal assemblages of decapod larvae for the subtropical waters of the Canary Islands. Despite significant inter-year differences in diversity and larval abundance, there were no evident changes in the larval assemblages. The detection of such changes in the community requires a multiyear dataset obtained in long-term monitoring programmes (Lindley et al. 2010Lindley J.A., Beaugrand G., Luczak C., et al. 2010. Warm-water decapods and the trophic amplification of climate in the North Sea. Biol. Lett. 6: 773-776.). This may be important, because the temporal distribution of spawning of different species is likely to vary under climate change.

Since 1997 the sea surface temperature has undergone a warming trend of 0.25°C decade–1 in the Canary Islands region (Vélez-Belchí et al. 2015Vélez-Belchí P., González M., Pérez-Hernández M.D., et al. 2015. Internannual, interdecadal and long-term variability. Open ocean temperature and salinity trends in the Canary Current large marine ecosystem. In Valdés L., Déniz-González D. (ed), Oceanographic and Biological Features in the Canary Current Large Marine Ecosystem, IOC-UNESCO, Paris. IOC Tech. Ser. 115: 299-308.), but little is known about subsequent alterations in breeding success and distribution of crustacean species. However, there is already clear evidence of a tropicalization in the Canary Islands ecosystems. For instance, many of the new records of fish (Brito et al. 2005Brito A., Falcón J.M., Herrera R. 2005. Sobre la tropicalización reciente de la ictiofauna litoral de las islas Canarias y su relación con los cambios ambientales y actividades antrópicas. Vieraea 33: 515-525.), decapod crustaceans (González et al. 2017González J.A., Triay-Portella R., Escribano A., et al. 2017. Northernmost record of the pantropical portunid crab Cronius ruber in the eastern Atlantic (Canary Islands): natural range extension or human-mediated introduction? Sci. Mar. 81: 81-89.), other invertebrates (Brito 2008Brito A. 2008. Influencia del calentamiento global sobre la biodiversidad marina de las Islas Canarias. In: Afonso-Carrillo J. (ed.), Naturaleza amenazada por los cambios en el clima. Actas III Semana Científica Telesforo Bravo. IEHC, Puerto de la Cruz, pp. 141-161.) and algae (Afonso-Carrillo et al. 2006Afonso-Carrillo J., Sansón M., Sangil C. 2006. First report of Reticulocaulis mucosissimus (Naccariaceae, Rhodophyta) for the Atlantic Ocean. Cryptogamie Algol. 27: 255-264., 2007Afonso-Carrillo J., Sansón M., Sangil C., et al. 2007. New records of benthic marine algae from the Canary Islands (eastern Atlantic Ocean): morphology, taxonomy and distribution. Bot. Mar. 50: 119-127.) are tropical species. Also, the warming during recent decades has enabled species with tropical affinities to spread quickly across the archipelago (e.g. ephemeral benthic algae, Sangil et al. 2012Sangil C., Sansón M., Afonso-Carrillo J., et al. 2012. Changes in subtidal assemblages in a scenario of warming: Proliferations of ephemeral benthic algae in the Canary Islands (eastern Atlantic Ocean). Mar. Environ. Res. 77: 120-128.), or to increase their populations significantly due to more favourable and longer recruitment events (e.g. echinoid Diadema africana Rodríguez, Hernández and Clemente, 2010, Hernández et al. 2010Hernández J.C., Clemente S., Girard D., et al. 2010. Effect of temperature on settlement and postsettlement survival in a barrens-forming sea urchin. Mar. Ecol. Prog. Ser. 413: 69-80.). The successful establishment of the tropical hydrocoral Millepora sp. (Clemente et al. 2011Clemente S., Rodríguez A., Brito A., et al. 2011. On the occurrence of the hydrocoral Millepora (Hydrozoa: Milleporidae) in the subtropical eastern Atlantic (Canary Islands): is the colonization related to climatic events? Coral Reefs 30: 237-240.) is also noteworthy, as it suggests profound future changes in benthic communities if warming trends continue. We consider the establishment of long-term plankton sampling programmes in tropical-subtropical regions of the NE Atlantic to track these interannual alterations in phenology and non-native crustacean species occurrence, which are already visible in temperate regions (Kirby and Beaugrand 2009Kirby R.R., Beaugrand G. 2009. Trophic amplification of climate warming. Proc. R. Soc. Lond. Ser. B Biol. Sci. 276: 4095-4103., Lindley et al. 2010Lindley J.A., Beaugrand G., Luczak C., et al. 2010. Warm-water decapods and the trophic amplification of climate in the North Sea. Biol. Lett. 6: 773-776.), to be of paramount importance.

To detect northward distribution shifts of tropical species in relation to current and future conditions in the subtropical and temperate Atlantic, more accurate larval descriptions are needed. According to González (2016)González J.A. 2016. Brachyuran crabs (Crustacea: Decapoda) from the Canary Islands (eastern Atlantic): checklist, zoogeographic considerations, and conservation. Sci. Mar. 80: 89-102., at least 23 brachyuran benthic species occurring in the Canary Islands have their northern limit of distribution at this archipelago. However, from these species only the larval morphology of Stenorhynchus lanceolatus (which actually occurs also in Madeira) and Microcassiope minor (Dana, 1852) (which is present also in the Azores islands) are known, and are described by Paula and Cartaxana (1991)Paula J., Cartaxana A. 1991. Complete larval development of the spider crab Stenorhynchus lanceolatus (Brullé 1838) (Decapoda, Brachyura, Majidae), reared in the laboratory. Crustaceana 60: 113-122. and Clark et al. (2004)Clark P.F., Dionisio M.A., Costa A. 2004. Microcassiope minor (Dana, 1852): a description of the first stage zoea (Crustacea: Decapoda: Brachyura: Xanthidae). Medit. Mar. Sci. 5: 23-33., respectively. We therefore encourage the scientific community to continue to improve the taxonomic description of the larval morphology of decapod crustaceans following the current standards, especially of tropical species that are presently less studied.

ACKNOWLEDGEMENTSTop

The authors would like to thank all the members of the Biological Oceanography Research Unit of the Universidad de Las Palmas de Gran Canaria who participated in this difficult sampling programme, and S. Hernández-León, principal investigator of the project, for his continuous support. Special thanks are due to J.A. González for providing valuable information about decapod fauna in the Canary Islands and to S. De Grave for his advice during the estimation of the diversity index. The project ConAfrica (CTM2004-02319) of the Spanish Ministry of Science and Innovation funded this study. JML was supported by a postdoctoral fellowship from the Japan Society for Promotion of Science (PE16401).

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