Cuadernos de Investigación UNED (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015 233 Abundance patterns (1984-1987 / 1994-1998) of polychaete worms (Annelida) from an estuarine tidal flat, Pacific, Costa Rica José A. Vargas-Zamora1,2, Jeffrey A. Sibaja-Cordero1,2, Harlan K. Dean3 & Sylvia Solano-Ulate4 1. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Universidad de Costa Rica, 11501-2060, San José, Costa Rica. jose.vargas@ucr.ac.cr, jeffrey.sibaja@ucr.ac.cr 2. Escuela de Biología, Universidad de Costa Rica, 11501-2060, San José, Costa Rica. 3. Museum of Comparative Zoology, Harvard University. 26 Oxford St. Cambridge, MA. 02138. USA; harlandean@gmail.com 4. Escuela de Estudios Generales, Universidad de Costa Rica, 11501-2060, San José, Costa Rica; silvia.solano@ucr.ac.cr ABSTRACT: The objectives of this report are to provide an updated list of the annelid polychaete worm species found at a tropical estuarine intertidal flat, describe long term oscillations of 11 of the species, and the impact of red tides as evidenced by PCA. From 1984 to 1987 (49 dates) 14 sediment cores (17.7 cm2 – 15 cm deep) were collected per date at low tide from a 400 m2 muddy-sand plot in the Gulf of Nicoya estuary (10oN-85oW), Pacific, Costa Rica. All cores were fixed in Rose Bengal stained formalin and sieved thru a 500 micron mesh screen. A total of 43 species of polychaetes were found and distributed among 25 families and 6 600 individuals, of which 80% were represented by: Mediomastus californiensis (32.4%), Caraziella calafia (20.3%), Paraprionospio alata (9.2%), Scolotema tetraura (5.9%), Gymnonereis crosslandi (4.9%), Spiophanex duplex (3.8%), and Glycinde armigera (3.5%). M. californiensis was numerically dominant during most of the sampling dates. The Spionidae (6), Phyllodocidae (4), and Nereididae (3) were the more speciose polychaete families. Populations of all species were patchy in space and time. The abundance patterns of 11 species are illustrated for the 1984-1987 data set. These patterns may reflect declining populations at the beginning of 1984 perhaps influenced by the strong 1982-1983 ENSO event. During 1985 red tides may have in- fluenced the abundances of polychaetes as indicated by the results of a PCA. This is the first time that population patterns of nine species of intertidal polychaetes over a three year period, and the impact of red tides on these worms are reported for this region of the eastern Pacific. General Additive Models (GAM) were applied to the abundances of M. californiensis and P. alata found during 1984-1987 and to additional data from 1994 to 1996 (28 dates) The GAM approach confirmed eal- ier observations of seasonal oscillations of these species during 1984- 1987, but these trends were not found during 1994-1998. Previously unnoticed underlying patterns of unknown origin were also detected by the application of GAM. The theoretical framework needed for the interpretation of results from tropical benthic surveys could improve significantly from more long term monitoring. Long term abundance data is essential to evaluate the impacts of anthropogenic activities in estuaries. Key words: Macrofauna, infauna, intertidal, benthos, GAM, PCA, red tides. RESUMEN: Los objetivos de este estudio fueron el proveer una lista actualizada de las especies de gusanos anélidos poliquetos encontra- dos en una planicie tropical de entre-mareas, describir oscilaciones de largo plazo de 11 de esas especies y el impacto de mareas rojas evi- denciadas por el análisis de PCA. Desde 1984 a 1987 (49 fechas) 14 núcleos de sedimento (17.7 cm2 – 15 cm de profundidad) fueron co- lectados por fecha en marea baja en un sitio fangoso-arenoso de 400 m2 en el estuario del Golfo de Nicoya (10oN-85oW), Pacifico, Costa Rica. Todos los núcleos fueron fijados en formalina en agua de mar tenida con Rosa de Bengala y tamizados en una malla de 500 micras de poro. Se encontró un total de 43 especies de gusanos poliquetos distribui- dos entre 25 familias y 6 600 individuos, de los que un 80% estaban representados por: Mediomastus californiensis (32.4%), Caraziella ca- lafia (20.3%), Paraprionospio alata (9.2%), Scolotema tetraura (5.9%), Gymnonereis crosslandi (4.9%), Spiophanex duplex (3.8%) y Glycinde ar- migera (3.5%). M. californiensis fue numéricamente dominante durante la mayoria de las fechas de muestreo. Las Spionidae (6), Phyllodocidae (4), y Nereididae (3) fueron las familias de poliquetos con más especies. Las poblaciones de todas las especies fueron irregulares en el tiempo y en el espacio. Se ilustran los patrones de abundancia de 11 de las especies para el periodo 1984-1987. Estos patrones pueden reflejar po- blaciones en decadencia al inicio de 1984, tal vez influenciadas por el fuerte evento ENSO de 1982-1983. Durante 1985 las mareas rojas pue- den haber influenciado las abundancias de poliquetos según lo indi- can los resultados de un PCA. Esta es la primera vez para el Pacífico del Este que se ilustran las oscilaciones poblacionales de nueve especies de poliquetos de entre mareas a lo largo de un período de tres años, así como el impacto de las mareas rojas en estos gusanos. Se aplicó el análisis por Modelos Aditivos Generales (GAM) a las abundancias de M. californiensis y P. alata recolectados durante 1984-1987 y adicio- nalmente entre 1994 y 1996 (28 fechas). El enfoque GAM confirmó las observaciones anteriores sobre la estacionalidad de estas especies du- rante 1984-1987, pero estas tendencias no fueron encontradas durante 1994-1998. Mediante el uso de GAM fueron también detectados patro- nes de origen desconocido no notados anteriormente. El marco teórico necesario para la interpretación de los resultados de estudios bénticos tropicales puede mejorarse mediante la realización de más monitoreos a largo plazo. Datos de abundancia de largo plazo son esenciales para evaluar los impactos de actividades antropogénicas en estuarios. Palabras clave: Macrofauna, infauna, entre-mareas, bentos, GAM, PCA, mareas rojas. Received 16-vII-2015 • Corrected 17-VII-2015 • Accepted 21-VII-2015 Research Journal of the Costa Rican Distance Education University (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015234 From 1979 to 1983 ecological surveys were conducted in the Gulf of Nicoya estuary, Pacific coast of Costa Rica to provide baseline information in support of government management strategies (see references in vargas 1995, and vargas & Mata, 2004). These studies were followed by surveys (1984-1987 and 1994-1998) of an intertidal flat in the upper estuary. The results of the first survey were previously published by vargas (1987, 1988a,b, 1989, 1996) and the structure of this benthic community was discussed. More recently we have focused on the abundances of the main taxonomic groups found at the intertidal flat, including cephalochordates (vargas & Dean, 2010), echinoderms (vargas & Solano, 2011), mollusks (vargas- Zamora & Sibaja-Cordero, 2011), and crustaceans (vargas-Zamora, Sibaja-Cordero & vargas-Castillo (2012). The availability of user-friendly software and expanded computer memory facilitates the analyses of these data sets to find previously hidden patterns, or to confirm previously described patterns, as illustrated early by Stephenson, Williams & Cook (1970). One set of pro- grams to analyze temporal patterns is the Generalized Additive Models (GAM) which has been applied to tem- perate infaunal communities by Stoner, Manderson, & Pessutti, (2001) and Jennings, Nicholson, Dinmore & Lancaster, (2002) among others. The review of the meth- ods by Wood (2006) and by Wood, Goude & Shaw (2015) have facilitated its use. At tropical latitudes we used GAM to describe temporal oscillations of the molluscan and crustacean species from the Punta Morales flat (vargas- Zamora & Sibaja-Cordero, 2011; vargas-Zamora, Sibaja- Cordero & vargas-Castillo, 2012). Dean (2009) updated the list of polychate worms reported from Costa Rica. Polychaeta was the most important taxonomic group in terms of number of species at the Punta Morales flat (vargas, 1987, 1988a, 1889). Thus, a closer look of its pop- ulation patterns was in order. Therefore, the objective of this note is to make accesible an updated list of the poly- chaete species found at the flat, and the results of the application of GAM and multivariate statistical methods to the updated polychaete data set. MATERiAlS ANd METhodS Study site: The intertidal flat is located on the South shore of the Punta Morales peninsula on the mid-upper region of the Gulf of Nicoya estuary (10oN-85oW) Pacific coast of Costa Rica. The sand-mud flat is limited to the North by a white sand beach. Rocky outcrops and man- grove stands are also prominent features of the pen- insula (Fig. 1). A dry season (December to April) and a rainy season (May to November) mark the seasonal- ity of nutrient dynamics and water salinity, which have been described by Epifanio, Maurer & Dittel (1983) and voorhis Epifanio, Maurer, Dittel, & vargas (1983) as part of the ecological surveys mentioned before. Freshwater inputs from seasonal rains and runoff carried by the Tempisque and Tarcoles rivers (Fig. 1) produce strong vertical and horizontal salinity gradients that drive es- tuarine circulation. Near Punta Morales the Largarto river (Fig. 1) contributes suspended sediment loads during the rainy season. Field and laboratory methods: The sampling pro- tocols are outlined in vargas (1987, 1988a, 1989) and in vargas-Zamora & Sibaja-Cordero (2011). In summary 14 cores (17.7 cm2 – 15 cm long) were collected at monthly intervals from muddy sands during low tide (mean tidal range: 3 m), from a 400 m2 plot located 20 m from a sandy beach (Fig. 1). The original data set of vargas (1987, 1988a, 1989) was expanded with additional data from March- April, 1987, for a total of 49 dates (February, 1984 to April, 1987) and with data collected at the site by Solano-Ulate (2007) from July 1994 to September 1996 (28 dates) us- ing the same methodology. This sampling effort (77 dates) is unique in tropical intertidal soft-sediment stud- ies. At the laboratory core samples were fixed in Rose Fig. 1. Location of the study site at the Punta Morales peninsu- la, Gulf of Nicoya estuary (10o 04’N-84o 58’W), Pacific coast of Costa Rica. 1: Tempisque river. 2: Tárcoles river. 3: Lagarto river. 4. Marine field station. Gulf of Nicoya Pier Pta. Morales Estuary Costa Rica 10 º N 85º W Pacific Ocean Study site Sandy beach Mangroves Rocky shores Tidal flats at low tide 0 200 mPunta Morales Gulf of Nicoya Pacific Ocean 10º N 85º W 1 2 3 4 Cuadernos de Investigación UNED (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015 235 Bengal stained formalin in sea water and later sieved (500 micron mesh). Organisms were sorted and stored in ethanol filled shell vials. The original list (vargas, 1986) of polychaete species was updated based on Dean (2009) and by inspection of the collections of voucher speci- mens deposited at the Museum of Zoology (University of Costa Rica) and at the Museum of Comparative Zoology (Harvard University). The presently valid names of spe- cies correctly identified in vargas (1986), as well as those assigned to new taxa, were verified by accesing the web page w.w.w.WORMS (World Register of Marine Species). Statistical methods: A Principal Component Analysis (PCA) was conducted on the log 10 (x+1) transformed abundance data of the 43 polychaete taxa (1984-1987). Additionally, a two-way ANOSIM (Clarke & Warwick, 1994) of the same data based in the Euclidean distance, was done to test seasonal effects (as first factor) on the assemblage of polychaetes. As a second factor the data series was evaluated for changes before and after the red tide events that were frequent in the upper Gulf of Nicoya in 1985 and reported by viquez & Hargraves (1995) Temporal trends were analyzed for the two more abundant species found during all dates of the 1984- 1987 and 1996-1998 surveys (the capitellid Mediomastus californiensis and the spionid Paraprionospio alata) with the Generalized Additive Model (GAM) of the free mgcv package in The R Project for Statistical Computing, with abundances log 10 (x+1) transformed to homogenize variances (Stoner, Manderson, & Pessutti, 2001). The GAM was carried out with the subroutine quasi (Wood, 2006). The mean abundances per season (dry vs rainy, 95% con- fidence limits) of these species were computed also with log 10 (x+1) transformed data and back to the original scale for graphical display. RESUlTS Information on environmental data is included in vargas (1987, 1988, 1989, 1996), vargas & Solano (2011), and vargas-Zamora & Sibaja-Cordero (2011). In summa- ry, sediment composition of the sand-mud flat averaged 65% sand and 32% silt+clay. Seasonal trends in sediment and water temperatures were not found by vargas (1987, 1988a). Water temperatures above 30oC were charac- teristic of this region of the estuary, with a maximum of 40oC on April 1984 (vargas 1987). Water salinities during the survey ranged from as low as 22 ppt (rainy season of 1984) to 34 ppt (dry seasons). The reader is referred to the original work of Solano-Ulate (2007) for more infor- mation on the 1994-1998 macrofaunal survey. A total of 43 polychaete species were found at the site of which 15 species names (35%) were updated and eight taxa await further taxonomic work (Table 1). During the 1984-1987 survey the 43 species were represented TABLE 1 Left columns: codes for the 43 polychaete (Annelida: Polychaeta) species as identified by 1987. Codes 01-95 as in vargas (1986,1987,1988a,1989). Codes 102-122, this study. Original species identifications. Center and Right columns: updated (this study) species identifications, polychaete families and total number of individuals collected. Intertidal sand-mud flat, Gulf of Nicoya estuary, Pacific coast of Costa Rica 01 Pectinaria californiensis Hartman, 1941 P. californiensis Pectinaridae 106 02 Chone mollis (Bush, 1904) C. mollis Sabellidae 69 03 Nepthys monroi Hartman, 1950 N. monroi Nephtyidae 59 04 Paraprionospio pinnata (Ehlers, 1901) P. alata (Moore, 1923) Spionidae 606 05 Spiophanes soederstroemi Hartman, 1953 S. duplex (Chamberlin, 1919) Spionidae 252 06 Neanthes succinea (Frey & Leuckart, 1847) N. succinea Nereididae 152 07 Neanthes sp. 2. Neanthes micromma Harper, 1979 Nereididae 3 08 Neanthes sp. 3. Nereis costaricaensis Dean, 2001 Nereididae 7 09 Armandia salvadoriana Hartmann-Schroeder, 1956 A. salvadoriana Opheliidae 84 10 Diopatra ornata (Moore, 1911) D. ornata Onuphidae 19 11 Acesta lopezi (Reish, 1968) Aricidia (Admira) lopezi Paraonidae 88 12 Notomastus hemipodus Hartman, 1947 N. hemipodus Capitellidae 46 13 Mediomastus californiensis Hartman, 1944 M. californiensis Capitellidae 2 140 14 Tharyx parvus Berkeley, 1924 Monticellina acunai Dean, 2009 Cirratulidae 69 15 Glycinde armigera Moore, 1911 G. armigera Goniadidae 235 16 Hemipodus borealis Johnson, 1901 Hemipoda pustatula (Friedrich, 1956) Glyceridae 4 Research Journal of the Costa Rican Distance Education University (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015236 by a total of 6 600 individuals collected in a total sample area of 1.21 m2. The 43 polychaete species were distrib- uted among 25 families (Table 1), with the Spionidae (6), Phyllodocidae (4), and Nereididae (3) as the most spe- ciose families. Six species were represented by a single individual and the following seven comprised 80% (Table 1) of the total number of individuals: the capitellid Mediomastus californiensis (2140 ind., 32.4%), the spionids Caraziella calafia (1338 ind., 20.3%), Paraprionospio alata (606 ind., 9.2%) and Spiophanex duplex (252 ind., 3.8%), the lumbrinerid Scolotema tetraura (394 ind., 5.9%), the nereidid Gymnonereis crosslandi (327 ind., 4.9%), and the goniadid Glycinde armigera (235 ind., 3.5%). The num- ber of species collected per date ranged from 10 to 23, and the number of polychaetes ranged from 47 to 397 (Table 2). The capitellid M. californiensis was the numeri- cally dominant worm for 34 of the 49 dates, followed by the spionids C. calafia (9 dates), P. alata (5) and S. duplex (1). Numerical dominance of M. californiensis ranged from 23 to 74 % (Table 2). From the 1994-1998 survey we focused here on the population oscillations of P. alata and M. californiensis only. Thus, the abundance fluctuations of these two poly- chaete worms during the 77 sampling dates are included in Figs. 2, 3, and 4 (Totals: 1078 cores, 1.90 m2 ). The abundance fluctuations of nine selected species from different families of worms are illustrated in Fig. 5. for the 1984-1987 survey. In general, abundances were patchy in time. However, higher abundances were ob- served during the first half of 1984 and declined after- wards, with the exception of P. delta which had a peak after the red tides of 1985. The spatial distribution among the 14 cores of these nine species, and those of M. cali- forniensis, C. calafia and P. alata, is illustrated in Table 3 for the date when the highest abundance of each species was found. Patchiness is space was also evident. Results of a Principal Components Analysis (Fig. 6) based on the abundances of the 43 species during 1984-1987 evidenced a change in the composition of TABLE 2 (Continued) 17 Goniada maculata Oersted, 1843 G. brunnea Treadwell, 1906 Goniadidae 22 18 Glycera americana Leidy, 1855 Goniada prosobranchia Böggemann & Fiege, 2001 Goniadidae 30 19 Lumbrineris tetraura Schmarda, 1861 Scoletoma tetraura (Moore, 1911) Lumbrineridae 394 20 Sigambra tentaculata (Treadwell, 1941) S. tentaculata Pilargidae 115 21 Genetyllis castanea (Marenzeller, 1879) Phyllodoce madeirensis (Langerhans, 1880) Phyllodocidae 10 22 Linopherus spiralis (Wesemberg-Lund, 1949) L. canariensis Langerhans, 1881 Amphinomidae 100 23 Cossura rostrata Fauchald, 1972 C. rostrata Cossuridae 28 24 Eteone aestuarina Hartmann-Schroeder, 1959 E. aestuarina Phyllodocidae 12 25 Ceratochephale crosslandi (Monro, 1933) Gymnonereis crosslandi (Monro, 1933) Nereididae 327 26 Prionospio delta Hartman, 1965 P. delta Spionidae 192 27 Polynoidae sp. 1. Polynoidae sp. 1 Polynoidae 1 28 Polynoidae sp. 2. Polynoidae sp. 2 Polynoidae 1 29 Spionidae sp. 5. Spionidae sp. 5 Spionidae 2 68 Syllidae sp. 1 Syllidae sp. 1 Syllidae 6 69 Magelona pacifica Monro, 1933 M. pacifica Magelonidae 37 78 Ampharetidae sp. 1 Ampharetidae sp. 1 Ampharetidae 4 82 Malacocerus vanderhorsti (Augener, 1927) M. indicus (Fauvel, 1928) Spionidae 12 84 Owenia collaris Hartman, 1955 O. collaris Oweniidae 5 85 Polydora citrona Hartman, 1941 Carazziela calafia Blake, 1979 Spionidae 1 338 88 Americonuphis reesei Fauchald, 1973 A. reesei Onuphidae 1 92 Arabellidae sp. 1 Oenonidae sp. 1 Oenonidae 2 95 Trochochaetidae sp. 1 Trochochaeta kirkegaardi Pettibone, 1976 Trochochaetidae 8 102 Pilargiidae sp. 2 Pilargiidae sp. 2 Pilarigiidae 13 108 Sternaspis scutata Ranzani, 1817 Sternaspis major Chamberlin, 1919 Sternaspidae 1 114 Hesionidae sp. 1 Hesionidae sp. 1 Hesionidae 7 116 Phyllodoce pseudoseriata Hartmann-Schroder,1959 P. nicoyensis Treadwell, 1928 Phyllodocidae 2 122 Phyllodoce lamellifera (Linnaeus, 1791) P. lamellifera Phyllodocidae 1 Total 6 600 Cuadernos de Investigación UNED (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015 237 the polychaete fauna: Dry season dates 1-6, and rainy season dates 10-16 of 1984 were grouped apart. Similar results occurred with rainy season dates of 1985 (28-34) and dry season dates of 1986 (33-38). Moreover, dates previous to the red tide events (starting around date 29) were scored at positive values of PC-1, and show less dis- persion on the axes than dates after the red tide event (gray shaded in Fig. 6). At around the mid rainy season of 1986 (date 42) the polychate composition became more similar (dates 43-49 grouped with pre blooms dates) to that of pre-red tide events. A two way ANOSIM indicated a small seasonal change in the composition of the poly- chaetes (R=0.10, p=0.022), and supported the changes after date 29 (June, 1985) when red tide events started (R=0.49, p<0.001). Results of the application of the General Additve Models to the M. californiensis 1984-1987 data indicates higher abundances during the dry season (Fig. 7A, B) of each year (F=17.75, d.f.=1, p=0.001) and confirmed ob- servations reported by vargas (1987,1988a,1989) but no additional temporal trend was found during the study period (F=0.16, d.f.=1, p=0.692) (Fig. 7C). During 1994- 1996, this species lacked seasonal peaks in abundance (F=2.18, d.f.=1, p=0.153)(Fig. 7D, E), but presented a long temporal trend (F=3.61, d.f.=3.4, p=0.024), with decreas- ing in abundances from July 1994 to December1995. Abundances increased again in later sampling dates (Fig. 7F). On the other hand, P. alata had peaks of abun- dance during the 1984-1987 rainy season (Fig. 8A, B) of each year (F=8.57, d.f.=1, p=0.005); and no additional temporal trends were found (F=0.86, d.f.=1, p=0.358) (Fig. 8C). During 1994-1996 no seasonal peaks were evident (F=2.14, d.f.=1, p=0.157) (Fig. 8D, E), but the population decreased from July of 1994 to December 1995, and then subsequently increased (F=3.61, d.f.=3.4, p=0.024), Fig. 8F. diSCUSSioN vargas (1987, 1988a, 1989, 1996) discussed the results of his survey of the intertidal benthos focusing on struc- tural aspects (fluctuations in the numbers of individuals and species in space and time) of the benthic commu- nity as an ecological unit. His research was followed by more detailed evaluations of the data sets focusing on the population dynamics of the main taxonomic groups found at the site (vargas & Dean, 2010; vargas & Solano, 2011; vargas-Zamora & Sibaja-Cordero, 2011; vargas- Zamora, Sibaja-Cordero & vargas-Castillo, 2012). In these later works the lists of 23 mollusks and 29 crustacean species were updated. The fauna also included several TABLE 2 Date code (1 to 49). Date (1984-1987).Total number of po- lychaete species (S). Total number of polychaete individuals (N). The species with the maximum number (n) of individuals and its code (as in Table 1). Percentage (%) of N represented by that species. Punta Morales sand-mud flat. Gulf of Nicoya estuary, Pacific. Costa Rica Date code Date S N n Code % 1 Feb. 22 12 142 85 13 60 2 Mar. 08 14 108 63 13 58 3 Mar. 20 13 167 67 13 40 4 Apr. 05 16 162 60 13 37 5 Apr. 17 13 165 60 13 36 6 May 03 11 113 55 13 31 7 May 16 13 72 29 13 40 8 Jun. 01 11 93 30 13 32 9 Jun. 19 11 62 24 13 38 10 Jul. 19 15 147 64 04 43 11 Jul. 31 20 164 44 04 27 12 Aug. 14 16 103 14 05 13 13 Aug. 28 16 109 28 13 25 14 Sep. 10 17 93 25 13 27 15 Sep. 27 16 140 43 13 30 16 Oct. 10 21 126 30 13 24 17 Oct. 26 14 90 23 04 25 18 Nov. 12 17 70 16 13 23 19 Nov. 24 17 54 15 13 27 20 Dec. 10 17 79 20 13 25 21 Dec. 26 18 107 40 13 37 22 Jan. 10 15 87 37 13 42 23 Jan. 24 18 92 33 13 36 24 Feb. 07 14 80 42 13 52 25 Feb. 21 16 106 50 13 47 26 Mar. 07 15 113 62 13 55 27 Apr. 10 13 160 118 13 74 28 May 09 13 174 110 13 63 29 Jun. 06 12 99 67 13 67 30 Aug. 19 17 132 34 04 25 31 Sep. 22 19 106 25 13 23 32 Oct. 16 15 203 76 85 37 33 Nov. 15 13 197 77 85 39 34 Dec. 16 13 150 75 85 50 35 Jan. 30 10 248 145 85 58 36 Feb. 13 12 385 285 85 74 37 Mar. 13 13 393 271 85 69 38 Apr. 29 11 397 273 85 68 39 May 26 12 86 33 85 38 40 Jun. 25 12 122 27 85 22 41 Jul. 24 18 114 26 04 23 42 Aug. 21 13 92 46 13 50 43 Sep. 19 14 94 37 13 39 44 Oct. 17 13 47 15 13 32 45 Dec. 02 15 101 57 13 56 46 Jan. 19 17 163 97 13 59 47 Feb. 20 23 114 48 13 42 48 Mar. 28 12 113 60 13 53 49 Apr. 29 10 66 25 13 38 Research Journal of the Costa Rican Distance Education University (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015238 Fig. 2. Numbers of Paraprionospio alata (gray bars) and Mediomastus californiensis (white bars). The extent of the rainy sea- son (lower salinities) is indicated. Gulf of Nicoya estuary, Pacific coast of Costa Rica. Punta Morales intertidal sand-mud flat. (February 1984 to February 1985). 100 80 60 40 20 0 Nu m be r o f i nd iv id ua ls / 1 4 co re s Sampling dates Fe b. 22 M ar. 08 M ar. 20 Ap r. 0 5 Ap r. 1 7 M ay 0 3 M ay 16 Ju n. 01 Ju n. 19 Ju l. 1 9 Ju l. 3 1 Au g. 14 Au g. 28 Se p. 10 Se p. 27 Oc t. 1 0 Oc t. 2 6 No v. 12 No v. 24 De c. 10 De c. 26 Ja n. 10 Ja n. 24 Fe b. 07 Fe b. 21 1984 1985 Rainy season Fig. 3. Numbers of Paraprionospio alata (gray bars) and Mediomastus californiensis (white bars). The extents of the rainy sea- sons (lower salinities) are indicated. Gulf of Nicoya estuary, Pacific coast of Costa Rica. Punta Morales intertidal sand-mud flat. (March 1985 to April 1987). 120 100 80 60 40 20 0N um be r o f i nd iv id ua ls / 14 c or es Sampling dates M ar. 07 Ap r. 1 0 M ay 09 Ju n. 06 Au g. 19 Se p. 22 Oc t. 1 6 No v. 15 De c. 16 Ja n. 30 Fe b. 13 M ar. 13 Ap r. 2 9 M ay 26 Ju n. 25 Ju l. 2 4 Au g. 21 Se p. 19 Oc t. 1 7 De c. 02 Ja n. 19 Fe b. 20 M ar. 28 Ap r. 2 9 1985 1986 1987 Rainy seasonRainy season species of flatworms, nemerteans, sipunculans, and a brachiopod (vargas, 1987, 1988a, 1989, 1996; Dittmann & vargas, 2001) During the 1984-1987 study an updated total of 43 species of polychaete worms were found dis- tributed among 6 600 individuals (Table 1) bringing the total number of known macrofaunal species collected by coring at the 400m2 plot to 112. During the 1994-1987 and 1994-1998 surveys Polychata was the most impor- tant group in terms of the number of species found at the intertidal flat. The updated list of polychaetes includes 15 name corrections (Table 1). Of particular importance are the updated names of the numerically dominant spio- nids, C. calafia, S. duplex, and P. alata, which were based mainly on Blake (1979), Meisner & Hutchings (2003), and Yokoyama (2005), respectively. However, eight spe- cies remain to be identified (Table 1) The relative impor- tance of these numbers of species and individuals in the context of discussions about tropical benthic diversity has been already addressed by Maurer & vargas (1984), Alongi (1989), Dittmann & vargas (2001) and Dittmann (2002), among others. A total of 317 species of polychaetes listed in the lit- erature for the Pacific coast of Costa Rica was reported by Dean (2009). He stated that the number of polychaetes from Central American coasts is lower when compared to other geographical regions, a fact that may be related to lower sampling efflort. Maurer,vargas, & Dean (1988) conducted a grab survey at 41 stations in the Gulf of Cuadernos de Investigación UNED (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015 239 Nicoya ranging in depths from 1 to 46 m and a total of 125 species (retained on a 500 micron mesh sieve) of polychaetes were identified. In the deep fjord-like Golfo Dulce estuary located south of the Gulf of Nicoya a to- tal of 47 polychaete species were collected in 139 corers (same core and mesh size as in this study) taken at nine stations ranging in depth from 43 to 200 m (León-Morales & vargas, 1998). On the Pacific coast of Central America, Molina-Lara & vargas-Zamora (1995) conducted an evaluation of the polychaete fauna at 15 stations along a shallow estuary in El Salvador (13oN) using the same coring device and mesh size as in this study and iden- tified 30 species. Dittmann & vargas (2001) compared the faunas of Punta Morales and El Salvador with those of similar habitats in Australia and although there were no polychaete species names in common certain species appear to be playing similar ecological roles at both sides of the Pacific. This similarity of ecological roles is interest- ing and a promising avenue for future research to under- stand how energy flows in tidal flats at different latitudes. Dominance by deposit feeders for instance was a feature in common between Australia and Central America. A feature of the Punta Morales polychaete assem- blage is the numerical dominance by the capitellid Mediomastus californiensis at 33 of the 49 dates (Table 2). M. californiensis, (a sub-surface deposit feeder) has been reported from both sides of the American Continent. For instance, Gaston, Lee & Nasci (1998) found no seasonal population trends in this species in a coastal lagoon on the Northern Gulf of Mexico, where it reached densi- ties ranging from 267 to 1258 individuals / 0.5 m2. If the maximum density of 118 individuals of M. californiensis / 0.0248 m2 (14 cores) included in Table 2 is extrapolated to 0.5 m2 a value of 237 ind. / 0.05 m2 is possible for Punta Morales. This number is similar to the minimum found in the coastal lagoon. M. californiensis has been reported by Weston (1990) as a deep burrowing (2-10 cm) worm that prefers shallow fine sandy sediments with low organic carbon content in waters of Puget Sound, Pacific coast of North America. At the Gulf of Nicoya M. californiensis was found at only 19 out of 41 subtidal grab station (Maurer & vargas, 1984). This low figure may indicate that shal- low and uneven grab penetration underestimated abun- dances. Cores taken in Punta Morales were cut at the 15 cm depth, which may have better sampled the popula- tion of this and other deep burrowing worms Dominance at other dates was due to numbers of the surface depostit feeding spionid polychates P. alata, S. du- plex and C. calafia (Table 2). Thus, the polychaete assem- blage of the Punta Morales sand-mud flat is dominated 10 20 30 40 50 60 70 Number of individuals / 14 cores Sa m pl in g da te s Jul. 22, 1994 Aug. 12 Aug. 26 Sep. 11 Sep. 22 Oct. 07 Oct. 22 Nov. 09 Nov. 22 Dec. 07 Jan. 04, 1995 Jan. 18 Feb. 01 Feb. 16 Mar. 15 Apr. 20 May 17 May 31 Jun. 29 Jul.19 Oct. 24 Dec. 12 Dec. 21 Jan. 10, 1996 May 06 Jun. 28 Aug. 05 Sep. 02 Ra in y se as on Ra in y se as on Ra in y se as on Fig. 4. Numbers of Paraprionospio alata (gray bars) and Mediomastus californiensis (white bars). The extents of the rainy seasons (lower salinities) are indicated. Gulf of Nicoya estuary, Pacific coast of Costa Rica. Punta Morales intertidal sand-mud flat. (July 1994 to September 1996). Research Journal of the Costa Rican Distance Education University (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015240 60 50 40 30 20 10 0 40 30 20 10 0 15 12 9 6 3 0 Feb. 22 Mar. 08 Mar. 20 Apr. 05 Apr. 17 May 03 May 16 Jun. 01 Jun. 19 Jul. 19 Jul. 31 Aug. 14 Aug. 28 Sep. 10 Sep. 27 Oct. 10 Oct. 26 Nov. 12 Nov. 24 Dec. 10 Dec. 26 Jan. 10 Jan. 24 Feb. 07 Feb. 21 Mar. 07 Apr. 10 May 09 Jun. 06 Aug. 19 Sep. 22 Oct. 16 Nov. 15 Dec. 16 Jan. 30 Feb. 13 Mar. 13 Apr. 29 May 26 Jun. 25 Jul. 24 Aug. 21 Sep. 19 Oct. 17 Dec. 02 Jan. 19 Feb. 20 Mar. 28 Apr. 29 Pe ct in ar ia ca lif or ni en si s ( n= 10 6) Ch on e m ol lis (n =5 9) N ep th ys m on ro i ( n= 59 ) G ly ci nd e ar m ig er a (n =2 35 ) Sc ol et om a te tr au ra (n =3 94 ) G ym no ne re is c ro ss la nd i ( n= 32 7) Pr io no sp io d el ta (n =1 92 ) Sp io ph an es d up le x (n =2 52 ) N ea nt he s s uc ci ne a (n =1 52 ) Number of individuals / 14 cores 19 84 19 85 19 86 19 87 Ra in y se as on Ra in y se as on Ra in y se as on Re d tid es Fi g. 5 . N um be rs o f n in e se le ct ed s pe ci es o f p ol yc ha et e w or m s. Th e ex te nt s of th e ra in y se as on s (lo w er s al in iti es ) a nd re d tid e ou tb re ak s ar e in di ca te d. . G ul f o f N ic oy a es - tu ar y, P ac ifi c co as t o f C os ta R ic a. P un ta M or al es s an d- m ud fl at (F eb ru ar y 19 84 to A pr il 19 87 , 4 9 da te s) . Cuadernos de Investigación UNED (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015 241 by surface and subsurface deposit feeding polychaete worms. However, it is relevant the presence of other less numerically important species that could play key struc- turing roles due to their feeding habits as carnivores, omnivores, and suspension feeders. This variety of roles indicates the presence of a relatively well organized food web. A literature survey on tropical flats from different latitudes was conducted by Dittmann (2002) who con- cluded that the occurrence of macrobenthic species ap- pears to be site specific and the composition of the local assemblages seems to be influenced by the presence of certain species (ecosystem enginneers) that through their living activities (tube building, construction of burrows, sediment reworking) influence the presence or absence of other species. Similarities between tidal flats seem to increase at higher taxonomic levels. Dittmann & vargas (2001) found that there were 26 genera, and 30 families in common be- tween Austrlia and Central America. A total of 25 families are included in Table 1. As a comparison, 35 polychaete families were found by Barrio-Frojan, Kendall, Paterson, Hawkins, Nimsantijaroen & Aryuthaka (2006) at five non- vegetated intertidal habitats in Thailand (9o N) in sedi- ments composed of similar percentages of sand (51 to 71%) to that of Punta Morales (65%). With the exception of the Pectinaridae and Trochochaeidae found in Punta Morales, the remaining 23 families were also found in Thailand. Moreover, in Thailand nine families were repre- sented by less than 5 individuals, while 10 families were so in Punta Morales. Both sedimentary environments were dominated by deposit feeders. The polychaete fauna of the Punta Morales estuarine intertidal sand-mud flat appears patchy both in time and space. Data included in Figs. 2, 3, 4 and 5 provide evidence of patchiness on a temporal scale, while data included in Table 3 do so at the spatial scale. Spatial patchiness may be due to several factors ranging from settling preferences of larvae to survival of individuals after predation or other disturbances (Thrush, 1991). This area of research remains little addressed in tropical benthic studies. Polychaete worms usually comprise the highest percentage of macroinvetebrates found in sedi- ment surveys and have quick population response to en- vironmental disturbances at least in temperate latitudes (see Gray & Elliot, 2010). The populations of polychaetes from the Punta Morales sand-mud flats may have reacted to two envi- ronmental disturbances of different spatial and temporal scales: At the regional scale and as previously discussed by vargas-Zamora, Sibaja-Cordero & vargas-Castillo (2012) sampling at the flat started in February 1984, sev- eral months after the strong (October 1982 - July 1983) El Niño Southern Oscillation (ENSO) high water tempera- tures returned to near normal values on the Pacific coast of Central America. The impact of this ENSO on sandy beach communities of Peru was reported by Arntz, Brey, Tarazona & Robles (1987). They found that invasions of macrobenthic species were more frequent during ENSO, and after November 1983 spionid polychaetes (Dispio and Scolelepis) became members of the community. The polychaete population patterns illustrated in Figs. 2, 3, 4, 5, 6, 7, 8 provide evidence in support of the hypothesis TABLE 3 Examples of spatial patchiness: species name and date with the maximum (within brackets) number of individuals found. Distribution of individuals among the 14 cores (core area 17.7 cm2 – core depth 15 cm). Punta Morales sand-mud flat. Gulf of Nicoya, Costa Rica. 1984-1987 Specie Date Total Cores 1 2 3 4 5 6 7 8 9 10 11 12 13 14 C. calafia Febr. 13, 1986 (285) 9 18 24 33 19 8 6 32 43 19 26 17 16 15 M. californiensis April 10,1985 (118) 10 13 15 10 8 9 0 4 5 5 9 14 6 10 P. alata July 19, 1984 (64) 5 6 4 1 7 2 3 12 3 3 3 9 3 3 P. delta April 29, 1986 (53) 8 1 5 15 4 1 9 3 0 2 2 0 2 1 S. duplex March 20, 1984 (42) 0 2 4 2 2 3 3 7 1 4 10 4 0 1 G. crosslandi April 29, 1986 (36) 1 1 0 5 2 2 4 3 4 9 3 2 0 0 S. tetraura April 17, 1984 (24) 2 1 3 0 2 3 1 2 5 3 0 0 2 0 G. armigera June 25, 1986 (18) 0 0 1 1 1 3 2 1 1 1 4 2 1 0 N. succinea Sept. 27, 1984 (15) 2 2 0 0 2 0 1 2 1 0 1 0 2 2 P. californiensis April 05, 1984 (14) 1 1 0 4 0 0 0 3 4 1 0 0 0 0 C. mollis July 19, 1984 (11) 0 0 0 0 1 0 7 1 1 1 0 0 0 0 N. monroi Febr. 22, 1984 (11) 2 2 1 0 0 0 1 0 0 2 2 1 0 0 Research Journal of the Costa Rican Distance Education University (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015242 Fig. 6. Principal Component Analysis (PCA) based on log 10 (x+1) transformed abundances of 43 species of polychate worms collec- ted during 49 dates (labelled 1 to 49). PC1, PC2 and PC3 explain 51 % of the variance. Squares (dry season dates), circles (rainy season dates). Gray shaded figures represent dates after the red tide outbreaks of 1985. All dates listed in Table 2. Gulf of Nicoya estuary, Pacific coast of Costa Rica. Punta Morales sand-mud flat, February 22, 1984 (Date 1) to April 29, 1987 (Date 49). Cuadernos de Investigación UNED (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015 243 that the benthic macrofauna of the Punta Morales flat was impacted by the 1982-1983 ENSO. Abundances during the first sampling months are indicative of de- clining populations. Higher abundances of flatwormrs, ostracods, and cumaceans were also found early in 1984 and declined afterwards (vargas, 1987; vargas-Zamora, Sibaja-Cordero & vargas-Castillo, 2012), However, these changes were not as evident with the mollusks (vargas- Zamora & Sibaja Cordero, 2011). At the Gulf of Nicoya scale the Punta Morales data set provide evidence of the response of the polychaete assemblage to an environmental disturbance that took place in this estuary in 1985. The results of a PCA (Fig. 6) indicate that a change in polychaete diversity and abundance is evidenced by the separation of the sets of cores collected in May and June, 1985 (dates 28 and 29) from the cluster of previous dates. This separation was clear by date 30 (August 19) and continued to around date 41 (July 24, 1986), when faunal composition returned to be similar to that of the dates from early 1985 and be- fore. Of particular relevance to the observed changes in the polychate assemblage detected by PCA are the ocur- rences from June to November (rainy season) of 1985 of red tide patches in the mid upper Gulf of Nicoya. viquez & Hargraves (1995) described the occurence of dinoflagellate bloms (Cochlodinium catenatum, Gymnodinium catenatum, and the non-toxic Prorocentrum balticum) in the Gulf of Nicoya estuary from January Fig. 7. Outputs of the Generalized Additive Models (GAM) for the abundances of the capitellid Mediomastus californiensis (1984- 1987, 49 dates). d, E, F: (1994-1996, 28 dates). A, d: Seasonal (dry vs rainy) mean abundance with 95% confidence limits. B, E: Seasonal effect. C, F: Remnant long term temporal trend. Solid line is the fitted value for the model. Broken lines are the Bayesian credible intervals. Dark bars at the bottom = rainy seasons. Punta Morales sand-mud flat, Gulf of Nicoya estuary, Pacific, Costa Rica. Research Journal of the Costa Rican Distance Education University (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015244 1985 to March 1986. These patches were frequent and dominated by C. catenatum until November, when G. catenatum became dominant. Dense patches of C. cat- enatum were found within the Punta Morales estuary, a few hundred meters North from the intertidal flat (Fig. 1). Although no sediment disturbances were observed at the time, a few dying Tellina clams were found on the sediment surface on August, 1985 (vargas-Zamora & Sibaja-Cordero, 2011). Moreover, fish mortalities restrict- ed to species of the family Sciaenidae were reported in the inner Gulf of Nicoya during late September and mid October 1985 (Szelistowski & Garita. 1989). Red tides ap- parently also reduced the densities of eggs and larvae of anchovies (Engraulidae) in and adjacent to the Punta Morales estuary (Ramírez, Szelistowski & López, 1989) The impact of microalgal blooms on the benthos has been reported previously only from a few locations in tem- perate and subtropical latitudes. The results of the PCA based on polychaete abundances at the Punta Morales site are the first for this region of the tropical Pacific. Dauer & Simon (1976) studied the impact of the 1971 dinoflagellate (Gymnodinium breve) bloom which caused anaerobic conditions in waters of the shallow Tampa Bay. Florida (28oN). Among the 22 more abundant species, the bloom reduced the total numbers of individuals and species by 97% and 77%, respectively. Some species with important densities (ind/m2) in 1970 dissapeared (0 ind/ m2) after the 1971 event and were found again in 1973, for instance: the onuphids Onuphis eremita (283 ind. in 1970- 0 ind. after -3 ind. in 1973) and Diopatra cuprea Fig. 8. Outputs of the Generalized Additive Models (GAM) for the abundances of the spionid Paraprionospio alata (1984-1987, 49 da- tes). d, E, F: (1994-1996, 28 dates). A, d: Seasonal (dry vs rainy) mean abundance with 95% confidence limits. B, E: Seasonal effect. C, F: Remnant long term temporal trend. Solid line is the fitted value for the model. Broken lines are the Bayesian credible intervals. Dark bars at the bottom = rainy seasons. Punta Morales sand-mud flat, Gulf of Nicoya estuary, Pacific, Costa Rica. Cuadernos de Investigación UNED (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015 245 (81-0-1), the nereidid Nereis succinea (33-7-3), and the glycerids Glycera capitata (16-0-2) and G. ameriana (3-0- 45). Species like Scolelepis texana had a diffeent patern (16-13-2). A total of 54 polychate species was found dur- ing their study and nine of them represented 79.6% of the total number of individuals. Among these nine spe- cies, Paraprionospio pinnata, Polydora ligni, Nereis suc- cinea, Magelona pettiboneae, Eteone heteropoda and Capitita ambiseta, have representative genera in the Punta Morales intertidal flat (Table 1), indicating similar trophic roles of the polychaete assemblages. Olsgard (1993) found significant reductions in the number of individuals and species in one year following a bloom of a toxic dinoflagellate (Chrysochromulina polyl- epis) in the coastal waters of Norway (580N). The change in faunal composition of the subtidal benthos became evident after a multivariate technique (DCA) was applied to the data set. This technique separated his data sets of 1987-1988 from those of 1989-1990. DCA also placed the 1990 set closer to that of 1987, indicating a tenden- cy of the fauna to return to pre-bloom struture. When abundances before and after the bloom were com- pared, certain polychaete species showed reductions in abundance ranging from 25 to more than 80%. After the bloom many species of polychaetes present in low numbers dissapeared from more of 30% of the stations sampled. The capitellid Heteromastus filiformis was first among the ten more abundant species during the study period and this rank was not affected by the bloom. No increases in abundance of opportunistic species (includ- ing H. filiformis and Spiophanes kroyeri) was observed af- ter the bloom. Wear & Gardner (2001) studied the impact of the 1998 bloom caused by the toxins of the naked dinoflagel- late Karenia brevisulcata in Wellington Harbour (41o S), New Zealand. They found that the four main groups of organisms (polychaetes, mollusks, crustaceans and echi- noderms) were equally affected. However, at one of the subtidal (11 m) stations at the entrance to the harbour the polychaetes were affected most, in comparison with the other three groups that had small increases or decre- ses in the number of individuals or species. In this con- text it is noteworthy that the spionid P. delta reached its peak of abundance in Punta Morales after the red tide oubreaks (Fig. 5). Of special interest are the oscillations in abundance of the spionid Polydora citrona (now Carazziela calafia, Table 1) described by vargas (1989) C. calafia was first recorded at the site in December of 1984 (3 individuals) and appeared sporadically until September 1985, when numbers increased from 18 to peaks of 145, 285, 271, and 273 individuals in January, February, March and April of 1986, respectively. Numbers declined to 33 by May and returned to single digits by August, 1986. It is note- worthy that numbers of this spionid started to increase late (June to November of 1985) during the period of red tides and reached its maximum several months later. At the micro-scale level no significant changes in abundance of C. calafia were evident in response to the deployment of wire mesh cages on the sediment dur- ing the dry (Totals: 7 ind. outside vs 9 ind. inside) and rainy (Totals: 247 outside vs 147 inside) seasons of 1985 (vargas, 1988a, 1996) Several species of the Spionidae and Capitellidae polychaete families are known to in- crease in abundance (Table 4A) in temperate latitudes in- side wire mesh cages deployed to ameliorate the impact of macro-predators (see Reise, 1985). At the tropical site, however, the population changes inside vs outside cages of the spionid P. alata and the capitellid M. californienesis were negligible (Table 4B). In addition to these disturbances the Gulf of Nicoya and its biota is under the influence of the more predict- able seasonal salinity cycle. vargas (1987, 1988) indi- cated that the whole benthic macrofaunal community had a seasonal response as evidenced by the results of Cluster and Multiple Discriminant Analysis. Moreover, at the population level several species presented seasonal oscillations, being more evident in M. californiensis and P. alata. Three main results of the application of General Additive Models (GAM) analysis to the abundances of M. californiensis and P. alata (Figs. 7, 8) during the pe- riod of 1984-1987 and 1994-1998 were obtained: First, it confirmed vargas (1987, 1998) observations that M. californiesis was more abundant during the dry seasons, while P. alata was so during the rainy seasons. Second: seasonality of these species was not detected in the 1994-1996 data set. Third: previously unnoticed under- lying patterns of unknown origin were detected by the application of GAM. Most of the ecological theories that guide the inter- pretation of the results of marine sediment surveys have been developed based on data from temperate latitudes. The books by Little (2000) on soft shores and estuarine habitats, and by Gray & Ellliot (2010) on marine sedi- ments in general address those theories. A better under- standing of the ecology of tropical benthos could benefit from more long-term monitoring and the aplication of user-friendly statistical methods in search for patterns. Data collected over periods of more than a year continue to be rare in tropical marine benthic literature. Moreover, climatic change and increased costal development make these data highly valuable for future comparisons. The Research Journal of the Costa Rican Distance Education University (ISSN: 1659-4266) Vol. 7(2): 233-248, Diciembre, 2015246 Gulf of Nicoya estuary has been heavily influenced by sedimentation, mangrove forest alteration, pollution, and fishery methods leading to bottom damage (shrimp trawling), removal of top predators (shark fishing) and extraction of filter-feeder shellfish (vargas & Mata, 2004). Borja, Dauer & Elliott (2010) point out that recovery of es- tuarine components may take from less than five years to more than 25 depending on the nature of the impacted component. In this context a clear knowledge of the abundance patterns of polychaetes and other groups must be at hand to evaluate potential recoveries after stressors have been removed or their effects ameloriated. ACKNowlEdgEMENTS This research was made possible by a grant from the Universidad de Costa Rica to project 808 - B3 - 113: El ben- tos de Punta Morales – 30 años después. REFERENCES Alongi, D. M. (1989). 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