Cross-Shelf Habitat-Fish Associations in La Parguera, Puerto Rico: Factors Affecting Essential Fish Habitat and Management Applications

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KIMBERLY A. FOLEY1, 2 and RICHARD S. APPELDOORN1 1University of Puerto Rico-Mayagüez, Isla Magueyes Marine Station La Parguera, Puerto Rico 00681 2Current address: University of South Carolina Baruch Marine Field Laboratory Georgetown, South Carolina 29442

ABSTRACT In accordance with the federal amendment to the Magnuson-Stevens Fishery Conservation and Management Act in 1996, it is critical that essential fish habitat (EFH) be identified for the conservation of declining fishery stocks. This study in La Parguera, PR used a habitat classification model along an inshore gradient, in conjunction with relative physical and structural reef attributes to identify associations between habitat and locally abundant reef fishes. The combination of benthic habitat, physical regime and structural characteristics offered a determination of EFH with regard to the local commercial species. A total of 35 species were included in Detrended Correspondence Analyses (DCA) to identify species com- plexes at varying spatial scales, both within and among shelf strata. Leeward zones were found to be highly unique, relative to the intermediate and windward zones of each stratum, due to a high abundance of sea grass habitat which support com- mercially important species. The physical attributes distinguished cross-shelf strata from one another, while habitat classifications distinguished exposure zones across strata from one another. Rugosity and structural complexity supported the distinction of exposure zones across strata from one another. Results presented enforce the fact that EFH cannot be a measure of simply benthic cover, but is a complex interaction of physical and biological factors influenced by reef location and position. The model employed in this study to identify EFH from the perspective of physical and biological factors can be locally adapted to further manage and protect marine habitats and their associated fisheries stocks.

KEY WORDS: Habitat classification, water motion, essential fish habitat

Asociaciones de los Hábitat para Peces a través de la Plataforma en La Parguera, Puerto Rico: Factores que Afectan el Hábitat Esencial para Peces y sus Aplicaciones en el Manejo

La enmienda de 1996 al acta federal para la conservación y manejo de pesca, Magnuson Stevens, requiere la identifica- ción y conservación de hábitat esencial (EFH) para la protección de poblaciones sobreexplotadas. El presente estudio reali- zado en La Parguera, PR utilizó un modelo para la clasificación de hábitat a lo largo del gradiente costero. El modelo inclu- ye características oceanográficas y estructurales del arrecife para identificar asociaciones entre hábitat y especies arrecífales. La combinación de características oceanográficas, estructurales, junto con asociaciones bénticas dominantes ofrecen clasificaciones efectivas de hábitat esencial (EFH) para peces de importancia comercial. Un total de 35 especies fueron incluidas en el análisis, “Detrended Correspondence Analyses” (DCA). Este tipo de análisis permite la identificación de asociaciones de especies a distintas escalas espaciales entre estratos de la plataforma arrecífal. Zonas orientadas a sotavento proseen asociaciones distintas a zonas intermedias o de barlovento, debido a la alta abundancia de yerbas marinas. Los atributos ocea- nográficos separan los estratos a través de la plataforma arrecífal, mientras que las clasificaciones de hábitats resultantes distinguen los de acuerdo a su exposición dentro de los estratos. De esta manera la complejidad topográfica del fondo dis- tingue asociaciones a lo largo del estrato de acuerdo a su nivel de exposición. Los resultados demuestran que EFH no puede ser medido en términos de cobertura biológica del fondo, sino que es una compleja interacción de factores físicos y biológi- cos afectados a su vez por la posición del arrecife a lo largo del gradiente de la plataforma. El modelo puede ser adaptado a otras localidades y ser una herramienta efectiva en la identificación y conservación de hábitats marinos y las poblaciones pesqueras asociadas con ellos.

PALABRAS CLAVES: Clasificación de los hábitat, movimiento del agua, hábitat esencial para peces

INTRODUCTION studies suggest that MPA site selection be reevaluated to Marine protected areas (MPAs) are recognized as include a mosaic of essential fish habitats to most effec- effective management tools for the protection of declining tively conserve open populations, such as coral reef fishes, fisheries stocks and associated habitats (Roberts and and their associated life stages (Appeldoorn et al. 2003, Polunin 1991, Bohnsack 1996). Recent benthic habitat Christensen et al. 2003). A single species may use several Page 22 58th Gulf and Caribbean Fisheries Institute benthic habitats for varied purposes: settlement (Booth and terrestrial corridors (Hobbs 1992), they exhibit sharp Beretta 1994, Danilowicz 1996), migratory feeding (Burke boundaries and dramatic habitat transitions within a small 1995, Friedlander and Parrish 1998) or refuge (Hobson area. To further investigate the influence of exposure on 1982, Holbrook and Schmitt 1988), for example. fish distributions, sites were classified into one of three Reef fish distribution is primarily influenced by exposure zones: Windward, Intermediate, or Leeward. The several key characteristics of benthic habitat: structural Windward zone included the area most exposed to complexity (Luckhurst and Luckhurst 1978), topographic incoming waves and currents, while the leeward side was relief (Williams 1982, Williams and Hatcher 1983, Roberts the most sheltered. and Ormond 1987, Yoshioka and Yoshioka 1989, Fried- Two reef sites, ~ 1.5 km from shore, were selected lander and Parrish 1998, Chabanet et al. 1997), and wave within the Inner shelf stratum, Collado and Las Pelotas and current regime (Kimmel 1985a, McGehee 1992, Green (Figures 1: 1 and 2). The Middle Shelf site, Enrique 1996). (Figure 1: 3), is a large intermediate reef 2 km from shore There is a lack of information combining these factors encompassing a significant portion of the middle shelf; to explain relationships between ambient parameters and therefore, there was no replicate in this stratum. The Outer habitat composition (Appeldoorn et al. 2003, Christensen Shelf sites, Laurel and Media Luna (Figure 1: 4 and 5) are et al. 2003). Few studies have attempted to compile these 3.5 km from shore and form the last emergent reefs line factors simultaneously and answer how they collectively before the shelf edge. influence fish distribution (Foley 2003) let alone test Reef sites were surveyed prior to data collection to influences at varying spatial scales. note homogenous habitat patches at the scale of 100 m2, This study used a structured hierarchal sampling and boundaries between patches. Sampling was designed design to investigate benthic habitat, structural attributes of to ensure that the complete array of homogeneous habitat habitat and physical regime along a cross shelf gradient patches was sampled. Microhabitat mapping (1 m2 within the insular shelf of La Parguera and determine to minimum mapping unit) followed Recksiek et al. (2001). what degree the factors influence reef fish distribution. Transects (24 x 4 m = 96 m2) were distributed randomly within patches. Some patches were only large enough to METHODS support but one transect without overlap. Thus, spatial La Parguera lies along the southwestern coast of habitat abundance determined whether replication was Puerto Rico and is comprised of three lines of emergent possible. reefs (Figure 1). Three cross-shelf strata (Inner, Middle Microhabitat classification included 20 categories of and Outer Shelf) were selected based on local measure- benthic cover (Table 1). Each microhabitat type was ments of bathymetry and expected co-variations in ranked based on relative characteristics of vertical relief salinity, turbidity, and wave exposure (Morelock et al. and were used to estimate structural complexity – an index 1977, Kimmel 1985a, Appeldoorn et al. 2001, Recksiek et of larger scale relief. High ranks correspond to microhabi- al. 2001). tats with a complex structure (e.g., Coral High Relief), while low ranks represent a more simple structure (e.g., Sand-Coarse). The index of Structural Complexity for a 500 m site corresponded to the sum of the proportional area of each microhabitat within that site multiplied by the Inner Shelf Stratum microhabitat rank. A smaller scale index of relieve was surface rugosity Middle Shelf Stratum (SR), measured using the chain method (Luckhurst and 2 Luckhurst 1978). Rugosity differs from structural 3 complexity in that certain types of relief (e.g., gorgonians) 1 1 are included in the latter, but not the former index. Six 4 Outer Shelf Stratum independent 3-m segments were sampled for each transect 5 and averaged. Transect means were pooled according to spatial classifications (strata and zones). Indices were tested with ANOVA (α = 0.05) and multiple comparison tests (α = 0.05), when applicable. Figure 1. Map of study site and reefs sampled along SW Relative measurements of water motion were made coast of Puerto Rico. using the copper-zinc corrosion method of McGehee (1998), with units placed near transect locations and clear Sampling focused on the channel axes, defined as the of obstructions at a depth of 1 - 4 meters. Measurements shallow lateral margins of emergent reefs where low to were made in February and again in May. Data from high wave gradients are prominent (Lindeman 1997). different reefs were pooled by stratum. Mean difference Channel axes provide excellent sampling sites because, like among strata and exposure zones were tested with ANOVA Foley, K.A. and R.S. Appeldoorn GCFI:58 (2007) Page 23

Table 1. Microhabitat types, codes and rank of structural complexity.

Code Rank Habitat Type Definition GT 2 Grass-Thalassia T. testudinum, no structural invertebrates. GS 2 Grass-Syringodium S. filiforme, no structural invertebrates. GM 2 Grass-Mixed Mixed grass, no discernible dominate species. GA 2 Grass with Algae Mixed grass, with attached/detached algae (e.g. Dictyota sp., Ulva lactuca). GI 3 Grass w/Small Invertebrates Sea grass with “small” invertebrates, (e.g., Favia fragum , sponges, or zooanthids). GL 4 Grass w/Large Invertebrates Sea grass with “large” invertebrates, (e.g., Acropora cervicornis, or brain corals) AA 2 Algae Algae of any species, or form. SC 1 Sand-Coarse Coarse sand composition. SF 1 Sand-Fine Fine sand composition. RB 3 Rubble Coral pieces/fragments. (Live/dead, original structure not intact). DL 4 Dead Coral-Low Relief Dead coral of simple structure, original framework intact. ML 6 Mixed-Low-Relief A mix, no one type dominates. Structure is simple with low relief. CL 6 Coral-Low-Relief Live corals (usu. smooth, flat or rounded Species, simple structure (e.g., Montastrea sp.) IS 5 Invertebrate Sponge Large barrel sponges and encrusting sponge colonies (e.g., Cliona sp.) CG 6 Coral-Gorgonian Gorgonians, often attached to hard structure DH 7 Dead Coral-High Relief Dead, branching species, original structure intact (e.g., Acropora cervicornis skeleton). MH 7 Mixed-High-Relief Mixed, no type dominates. Complex structure CH 7 Coral-High Relief Live branching species with complex structure. (e.g., Acropora cervicornis, Porites porites) and multiple comparison tests when applicable (α = 0.05). followed similar but separate arcs of increasing values A restricted list of 35 species (Table 2) was surveyed, along each axis from Leeward to Windward, with the Inner based on the following criteria: stratum located farther to the left, indicative of lower i) Commercial importance, complexity. The arc connecting Middle stratum sites was ii) Trophic significance, more irregular, with the Middle Intermediate having high iii) Movement, complexity, despite low rugosity and low water motion. iv) Non-cryptic, and Patterns in the Middle stratum, in general, tended to depart v) Locally abundant. from expectations, with (1) a lower overall level of water flow, (2) the lowest flow in the Intermediate zone, and (3) Visual census (Recksiek et al. 2001) was conducted a pattern where the variability in rugosity increased from over the previously mapped transects. All individuals were Leeward to Windward, the opposite to that observed in the identified, counted, and their microhabitat association other two strata. recorded as the position located on the habitat map. A total area of 8,736 m2 was surveyed among the five Mean species densities and microhabitat densities were reefs (Table 1). Four microhabitats were not noted in any calculated for cross-shelf strata and exposure zones. surveys: Grass-Syringodium, Sand-Fine Grain, Mangrove Detrended Correspondence Analysis (DCA) was per- and Detached Macrophytic Algae. A DCA based on formed using fish density and microhabitat density data to microhabitat densities within each stratum/exposure zone characterize communities by strata and zone (Hill and (Figure 3) showed that the grass habitats were grouped Gauch 1980). together by their dominance in the Inner stratum and Leeward zones of strata. Dead coral of high and low relief RESULTS (DH and DL) plotted centrally as ubiquitous microhabitats Comparing all sites (Figure 2), the relationship among and Invertebrate-sponge habitat (IS) was only found in the the principal environmental factors measured (water flow, Outer stratum. The graph shows separation by exposure rugosity and structural complexity) that potentially affect along the diagonal, with Leeward habitats to the lower left fish community structure was complex, yet certain patterns and windward habitats to the upper right. Along the were observed. The Leeward zones within each stratum opposite diagonal, the Inner Shelf stratum was separated are different from the other exposure zones and thus (upper left) with no clear separation of Outer and Middle displaced to the left, all characterized by low rugosity and strata. complexity. Sites within the Outer and Inner strata Page 24 58th Gulf and Caribbean Fisheries Institute

Table 2. Scientific and common names of species with corresponding codes. Species Name Family Code Common Name Acanthurus bahianus Acanthuridae Aba Ocean surgeonfish Acanthurus chirurgus Acanthuridae Ach Doctorfish Acanthurus coeruleus Acanthuridae Aco Blue Tang Abudefduf saxatilis Pomacentridae Asa Sergeant Major Abudefduf taurus Pomacentridae Ata Night Sergeant Caranx ruber Carangidae Cru Bar Jack Chromis multilineata Pomacentridae Cmu Brown chromis Haemulon carbonarium Haemulidae Hca Caesar grunt Haemulon chrysargyreum Haemulidae Hch Smallmouth grunt Haemulon flavolineatum Haemulidae Hfl French grunt Haemulon plumieri Haemulidae Hpl White grunt Haemulon sciurus Haemulidae Hsc Bluestriped grunt Haemulon striatum Haemulidae Hst Striped grunt Holocentrus adscensionis Holocentridae Has Squirrelfish Holocentrus rufus Holocentridae Hru Longspine squirrelfish Lutjanus apodus Lutjanidae Lap Schoolmaster Lutjanus griseus Lutjanidae Lgr Gray snapper Lutjanus synagris Lutjanidae Lsy Lane snapper Microspathodon chrysurus Pomacentridae Mch Yellowtail damselfish Mulliodichthys martinicus Mullidae Mma Yellow goatfish Ocyurus chrysurus Lutjanidae Och Yellowtail snapper Oligoplites saurus Carangidae Osa Leatherjacket Scarus iserti Scaridae Sis Striped parrotfish Scarus taeniopterus Scaridae Sta Princess parrotfish Sparisoma aurofrenatum Scaridae Sau Redband parrotfish Sparisoma chrysopterum Scaridae Sch Redtail parrotfish Sparisoma rubripinne Scaridae Sru Yellowtail parrotfish Sparisoma viride Scaridae Svi Stoplight parrotfish Sphyraena barracuda Scaridae Sba Great barracuda Stegastes diencaeus Pomacentridae Sdi Longfin damselfish Stegastes adustus Pomacentridae Sad Dusky damselfish Stegastes leucostictus Pomacentridae Sle Beaugregory Stegastes partitus Pomacentridae Spa Bicolor damselfish Stegastes planifrons Pomacentridae Spl Threespot damselfish Stegastes variabilis Pomacentridae Sva Cocoa damselfish

Figure 2. Three dimensional plots of Rugosity, Structural (Topographic) complexity and relative

water motion (zinc weight loss (g) for May). (For site codes: Out=Outer Shelf, Mid=Middle Shelf, Inner=Inner Shelf, Win = Windward zone, Int=Intermediate zone, Lee=Leeward zone).

Foley, K.A. and R.S. Appeldoorn GCFI:58 (2007) Page 25

A total of 18,426 fishes, from a select list of species Axis 1 than the Windward sites in the same stratum. (Table 2) were recorded among 91 transects. The Inner However, in the Middle Shelf the Windward site plotted stratum contained the highest mean fish density than of all lower on Axis 1 and higher on Axis 2 than the Intermediate strata, with > 50% of all fishes observed. Among exposure zone of this stratum. As a result, there was not such a clear zones across strata, mean fish density was highest in the distinction between the Middle and Outer Shelf Intermedi- Intermediate zone despite having the least number of ate and Windward sites as they plotted in a tight cluster (far species present. Among the stratum/exposure zones, right), sharing similar species densities. greatest mean density was found in the Inner Intermediate The DCA of species densities by microhabitat is seen site. in Figure 5. Species associated with sea grass habitats are In the DCA of species densities for exposure zones found toward the upper left, while species associated with within strata (Figure 4), ubiquitous species were found in a hard bottom habitats are found in the lower right. Few cluster at the center of the plot elongated along Axis 1. species-microhabitat associations were prevalent. Haemu- There was a clear distinction between the Leeward sites lon striatum and Lutjanus griseus were associated almost (upper left) and other zones, as well as between strata. The exclusively with coral high relief (CH) while Oligoplites Inner Shelf sites plotted in the lower left, the Middle Shelf saurus was strongly associated with seagrass-algal habitat sites are in the upper right and the Outer Shelf sites lie (GA). Interestingly, Scarus taeniopterus was associated along the diagonal in between. The pattern along Axis 1 with the small amount of IS in the Outer Shelf (3%), with within a stratum was not consistent. Within the Inner and the majority found in the Outer Windward. Outer strata, the Intermediate sites plotted lower along

2.0 Inner Int Inner Win

1.6

1.2 DH GL MH Middle Win

Axis 2 Axis DL 0.8 GI Outer Int GA GT AA SC CG Inner Lee Outer Win 0.4 CH IS GM RB ML CL

-1.5-1.0 -0.5 0.5 1.0 1.5 2.0 2.5 Middle Lee -0.4 Middle Int

-0.8 Outer Lee

-1.2

Axis 1

Figure 3. DCA plot of square root transformed habitat density of each stratum/ exposure zone. Eigenvalues: (1) 54.3 % (2) 13.1 %. (see Table 1 for habitat codes, Figure 2 for site codes).

Middle Lee 3.5 Hst Sva 2.8 Outer Lee Ata Middle Win 2.1

Axis 2 Och Sba Sle Sdi Sta Hfl Outer Int Middle Int Inner Lee Has Lgr Spa Mch 1.4 Hsc Sch Cmu Spl Svi Hca Hpl Sis Lsy Sad Sau Cru Aba Aco Asa Outer Win 0.7 Mma Sru Lap Osa Ach Hch Inner Win Hru

-0.7 0.7 1.4 2.1 2.8 3.5 Inner Int -0.7

Axis 1

Figure 4. DCA of species density by the nine stratum/ exposure zones. Ei- genvalues of axes: (1) 37.1 % and (2) 9.3 %. Page 26 58th Gulf and Caribbean Fisheries Institute

GAOsa GL GM3.4

GT Sba 2.7 Sch Och RB AA CG Aba Sva Cru SC GI Scr Sau 2.0 Hpl SruSle Hfl LsyAchDL Sta CL SviSdiSpa IS Hsc HruAcoSfu MH 1.4 MchHasSpl MmaLapAta Axis 2 HcaAsa DH 0.7 Cmu Hch ML Lgr CHHst -1.4-0.7 0.7 1.4 2.0 2.7 3.4 -0.7

-1.4 Axis 1

Figure 5. DCA of species density within habitats. Eigenvalues of axes were (1) 32.9 % and (2) 12.4 %.

DISCUSSION In the other two strata, grass habitats were less abundant Patterns of relative water motion, rugosity and and restricted to the Leeward exposure zones. structural complexity were complex. The expected pattern Combinations of habitat are important, and these may was one of decreasing water motion, rugosity and struc- also vary across the shelf. For example, coral habitats seen tural complexity Windward to Leeward within strata and within the Inner Shelf and Middle Shelf Leeward zones Outer to Inner Shelf across strata. The Middle Shelf site were due to patches of Acropora cervicornis. In the Inner consistently deviated from the expected pattern. This may Shelf, patches are small and scattered around sea grass in result from the actual patterns of current flow and waves the Leeward zone (where they are important for newly relative to the actual geomorphology (Foley 2003) or settled haemulids (Hill 2001), while the Middle Shelf patch simply be due to the lack of replication for the Middle consisted of a single large patch (~ 200 m2) among the sea Shelf site. grass near the reef crest. Haemulon striatum was observed Strong differences in microhabitat composition were in high density within the Middle Shelf Leeward site, found among reef lines and among exposure zones, leading exclusively within the “Thalassia-Acropora cervicornis to concomitant differences in fish communities. Neverthe- complex”; only four other individuals were observed less, the close association between water motion, rugosity outside this site. Thus, habitats with limited distribution and structural complexity as they varied across strata and become especially important within a stratum. This may zones indicates that fish may respond to a suite of factors. apply also to habitats outside the immediate area of study. This may explain why the Middle Shelf sites fell outside Mangrove stands were not surveyed within any of the Inner and Outer Shelf sites in Figure 3. channel axes, but occur in close proximity (150 m) to the Few exclusive preferences were noted among species Inner Shelf Leeward. This proximity likely influenced the and habitats, thereby not supporting habitat as the domi- sightings of smaller individuals that use mangroves as nant factor driving fish distribution. These results may nurseries (Hill 2001, Nagelkerken et al. 2002 Mumbry et differ from Christensen et al. (2003), who determined al. 2004). For example, Sphyraena barracuda, known to habitat type to be the greatest influence of distribution at use primarily mangroves as nursery areas (Murphy 2001, the family level, regardless of shelf position. This is a Aguilar-Perera 2004), was particularly associated with result of differences in scale, both spatial (minimum Inner Shelf sea grass habitats, likely swimming between mapping unit of 4,000 m2 vs. 1m2 in this study) and in the sea grass bed and mangrove habitats hunting small comparing associations at the family level versus species fishes. Only two other individuals (large adults) were level. Nevertheless, for many species, the combination of recorded (Middle Shelf Leeward and Outer Shelf Wind- habitat, even at the microscale, and shelf location may be ward). This proximity of mangroves may explain why important. For example, sea grass habitats proved observed densities in the Inner Leeward and Intermediate especially important in differentiating among shelf strata, zones were almost double those at other stratum-zone which in turn affected several species. All sea grass combinations. habitats (except Grass-Mixed in the Windward zone) were Under the U.S. Magnuson-Stevens Fishery Conserva- found among all exposure zones of the Inner Shelf stratum. tion and Management Act, essential fish habitat (EFH) Foley, K.A. and R.S. Appeldoorn GCFI:58 (2007) Page 27 must be identified for the conservation of declining fishery Christensen, J.D, C.F.G. Jeffrey, C. Caldow, M.E.Monaco, stocks. Marine Protected Areas (MPAs) are one of the M.S. Kendall, and R.S Appeldoorn. 2003. Cross- most useful tools to manage fish populations through Shelf Habitat Utilization Patterns of Reef Fishes in habitat protection and conservation. In this study, the Southwestern Puerto Rico. 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