Ecology of Three Sea Catfishes (Ariidae) in a Tropical Coastal Ecosystem - Southern Gulf of Mexico*

MARINE ECOLOGY PROGRESS SERIES Vol. 49: 215-230, 1988 - Published November 30 Mar. Ecol. Prog. Ser.

Ecology of three sea catfishes (Ariidae) in a tropical coastal ecosystem - Southern Gulf of Mexico*

Alejandro Yaiiez-Arancibia, Ana Laura Lara-Dominguez

Instituto de Ciencias del Mar y Lirnnologia, Universidad Nacional Autonoma de Mexico, Apartado postal 70305, 04510 Mexico, Distrito Federal, Mexico

ABSTRACT: Catfishes of the Family Ariidae are characterized as eurythermal and euryhallne inhabit- ants of estuarine waters. In the Southern Gulf of Mexico (Terminos Lagoon) there are 3 species: Arius felis, A. melanopus, and Bagre rnarinus. Juveniles of A. melanopus occur in the fluvial-lagoon system (FLS) in areas with oysters Crassostrea virginica, while adults occur throughout the lagoon. A. melanopusreaches sexual maturity at 160 mm total length (TL) and reproduces in FLS in salinities < 12 ppt, temperatures 2 35 "C and high turbidity waters. Males of 160 to 222 mm TL with eggs and/or embryos in their mouths are abundant in August and September, after which they migrate towards areas of greater salinity, lower temperature and less turbidity Juveniles recruit towards the western inlet (estuarine) and central basin of the lagoon. The reproduclve pattern of A. felis is the inverse of A. melanopus. Juveniles are found in areas of hgher salinity in the lagoon, and adults occur throughout the lagoon. The species matures sexually after reaching 200 mm TL and reproduces in salinities > 12 ppt, temperatures 2 30 "C, and in less turbid areas dominated by Thalassia testudi~~ummeadows. Males with eggs and/or embryos in their mouths are found In September. After the incubation period adults migrate toward the eastern inlet (marine)and luveniles toward the western inlet (estuarine). B. marjnus is found only in the western inlet (estuarine), central basin, and FLS of Terminos Lagoon. This specles reproduces along the coastline and enters the lagoon at the end of the rainy and winter storm or nortes season. Juveniles use the lagoon as nursery area. The Terminos Lagoon has a high diversity of habitats due to ecological interchange with rivers, swamps and the inner shelf. Three main strategies in the use of the system by catfishes in relation to reproduction and feeding may be characterized as: (1) spawning in the rivers and swamps followed by a migration of juveniles toward the central part of the estuarine system; (2) spawning in the estuarine system; and (3) spaw~ngin the sea followed by migration of juveniles to the FLS for feeding. Estuarine fish that have separate reproduction, growth, and feeding areas generally occur in great abundance and have adapted by reducing interspecific competition and temporal and spatial niche partition. In tropical high diversity ecosystems, biological cycles are closely related to high productivity of coastal waters, large supply of organic matter, increased food availability, and protection from predators. The estuary-inner shelf or swamp-estuary migrations can be interpreted as small-scale anadromous adaptations.

INTRODUCTION Mexico, including our study area, there are 3 species: in order of abundance Arius melanopus, A. felis and Bagre In tropical and subtropical America the family Ariidae marinus (e. g. Yafiez-Arancibia et al. 1976, Amezcua is one of the most abundant fish groups in coastal lagoons Linares 1977, Yafiez-Arancibia 1978, Yanez-Arancibia and estuaries. For example, on the Mexican Pacific coast et al. 1980, Lara-Dominguez et al. 1981). there are 13 species. Of these, Galeichtys (= An'us) Results of a number of studies indicate that sea caerulescens is the most abundant, while in the Gulf of catfishes are among the most abundant fishes in the Gulf of Mexico coastal zone (Sheridan et al. 1984, Deegan & ' Thompson 1985). Their morphological, reproductive, Contribution No. 456 from the Institute of Marine Sciences feeding, and migratory adaptations are closely linked to and Lmnology, Universidad Naclonal Autonoma de Mexico. Presented at the international symposium 'Comn~on physical processes and the heterogeneity of habitats in Strategies of Anadromous and Catadromous Fishes', Boston, estuarine lagoon systems. In the coastal zone, from USA, March 9-13, 1986, Am. Fish Soc. swamps and marshes to the inner shelf, there are coastal

O Inter-Research/Pnnted In F. R. Germany 216 Mar Ecol. Prog. Ser. 49. 215-230, 1988

lagoons and estuaries with permanent resident, migra- Puerto Real Inlet, to the west and east respectively of tory, cyclical, and occasional visitor species. This great Carmen Island) connect the lagoon to the sea (Fig. l), variety of life cycles indicates that estuarine fishes play and there is a strong westerly flow of water caused by an important role in the ecology of these ecosystems as a the predominantly southeasterly winds. Because of this form of energy storage within the ecosystem, and as circulation pattern, there are semipermanent gradients transformers and regulators of energy (Yanez-Arancibia of salinity, turbidity, nutrient levels, and sediment & Nugent 1977, Deegan & Thompson 1985, Yanez- types (Yanez-Arancibia & Day 1982, Yanez-Arancibia Arancibia 1985). The diurnal and seasonal utilization of et al. 1983). There are 3 climatic periods, the rainy these ecosystems by fish, together with separation of the season from June to September, the winter storm (nor- habitats for different life historystages, contributes to the tes) season from October to January, and the dry sea- high diversity in tropical estuaries. son from February to May. The southern part of the The objectives of our study on Anus felis, A. lagoon receives freshwater (6 X 10' m3 yrpl) from 3 melanopus, and Bagre marinus were (1)to determine main rivers. There is a great diversity of estuarine and compare the spatial-temporal pattern of distribu- habitats, including high and low salinity mangrove tion and abundance; (2) to establish time and place of swamps, seagrasses, marshes, high sedimentation spawning; and (3) to establish feedings habits. These areas, oyster reefs, and a mesohaline central basin. data are evaluated in relation to habitat requirements Five ecological areas are outlined in Fig. 1 and Table 1. of each species. Data on sea catfishes may be relevant Salinity is high (up to 30 %o)in the north and northeast for understanding the small-scale anadromy in tropical of the lagoon during the dry season. Benthic macroin- coastal ecosystems. Moreover, sea catfishes are species vertebrates and fish assemblages are specific for each with estuarine perspectives for future aquaculture. habitat and are controlled by salinity, fluvial input, turbidity and sediment types, detailed information on which is presented by Yaiiez-Arancibia & Day (1982) STUDY AREA and Yanez-Arancibia et al. (1980, 1982, 1983).

Terminos Lagoon is a large (ca 2500 km2), shallow (X = 3.5 m) lagoon in the Southern Gulf of Mexico border- METHODS ing Campeche Sound. The climate is humid tropical with an annual rainfall of 1100 to 2000 mm, and tidal Field activities. Fish were collected with a 5 m range is 0.3 to 0.7 m. Two inlets (Carmen Inlet and shrimp trawl (mouth opening while fishing was 2.5 m;

Fig. 1. Terminos Lagoon in the Southern Gulf of Mexico with the 5 habitats proposed for the estuanne lagoon ecosystem (see Table 1). Fish collection stations [l to 18 plus Estero Pargo Inlet (ESP) and Puerto Real 35 *I Inlet (PRI)] are shown for 1980 to 1982. Graphs show spatial variation in transparency (Ok) and salinity (ppt) in the 5 lagoonal habitats. Temporal variations in temperature ( C) and sal~nlty(ppt) are adapted from Day et al. (1C)82).Yanez-Arancibia & Day (1982), and Yancz-Arancibia et al. (1983) HABITATS MONTHS Table 1 Maln ecological charactenstics of habitats In Terminos Lagoon (from Yanez-Aranc~b~aet al. 1983)

Habltats Salinity (%o) Transparencyh (%) Water influenceC Observations

(Fig. 1) Mean (CV, '/U)" Mean (CV, %)" Sea Fresh

ECI Inner littoral of Carmen I+ Strong seawater influence. Similar to Habitat CB durlng Island dry season. Sand and silty-clay wlth 30 to 7OC%CaC03. Macroalgae seagrass meadows and mangrove swamps CB Central Basln 2+ Transition zone. Simllar to Habltat ECI during dry season and to Habitat FLS In nortes and ralny seasons. Muddy with [ine sand and clay-silly with 30 to 40"/0 CaC03. Macroalgae FLS Fluvial Lagoon Systems 4+ Strong riverine ~nfluence.Similar to Habltat CB dunng Eastern (FLS 1) dry season. Silty-clay with fine sand with 20 to 30% CaC03. Seagrass meadows, mangrove swamps and oyster reefs Western (FLS 2) 4+ Similar to Habit-at C1 during dry season. Sllty-clay wlth 20 to 30 % CaCOJ. Mangrove swamps and oyster reefs. During nortes and rainy season FLS 1, FLS 2 are simllar to Habitat CB C1 Carmen Inlet 3+ Variable zone due to marine and freshwater ~nteractlons. Similar to Habitat FLS 2 dunng dry season and to Habitats ECI and CB during nortes and rainy seasons. Clay-silty with less than 30% CaCO:,. hdangrove swamps and macroalgae debris PR1 Puerto Real Inlet l+ Predominantly marine due to the net flow of the Gulf of Mexico water toward the lagoon. Slmllar to Habitat ECI and with CB during dry season. Sand and s~lty-claywlth 50 to 70%" CaC03. Macroalgae, seagrass meadows, and mangrove swamps " CV: Coefficient of Variation = 100 SD/mean h Transparency has been estimated and related to the depth by T = (t/d)100 (where T = percentage of transparency; t = llght penetration lnto the water column, d = depth during each event) ' Magnitude of influence = 1+ to 4 + 218 Mar. Ecol. Prog. Ser. 49: 215-230, 1988

19 mm mesh), with drags of 10 to 12 min at 2 to 2.5 delimited by the gravimetric percentage, the percent- knots; individuals trawls covered an area of 1500 to age of frequency of occurrence, and the relative 2000 m'. Depths sampled varied but never exceeded importance index in logarithmic scale, and is sub- 3.5 m. Catches of sea catfish were made monthly from divided into 3 quadrants as follows. Quadrant I (ABCD) March 1980 to April 1981 at 18 sampling stations in the = area of occasional or circumstantial trophic groups of lagoon (Fig. 1). In addition, sea catfish were sampled relahvely little importance. This quadrant is defined by each 2 h over 24 h periods in Puerto Real Inlet (PRI) and a combined range of frequency and weight from 0 to in the entrance to Estero Pargo (ESP). In PRI, sampling 20 % and RI1 values from 0 to 10 %. Quadrant I1 was carried out during August, October, and December (DEFG) = area of trophic groups of relatively second- 1980, and February, April, June and July 1981; in ESP, ary importance. This quadrant has a combined range of fish were sampled during February, March, May, July, frequency and weight from 20 to 40 O/O and an RI1 range September and November 1981, and January 1982. of 10 to 40 O/O. Quadrant I11 (HIJK) = area of preferred or These 2 sampling locations were used in this study only main groups of relatively great importance, determined for spatial distribution and length frequency of the 3 by a combined range of frequency and volume or sea catfish for this study. Specimens were fixed in weight from 40 to 100 % and an RI1 range of 40 to 100. neutralized 10 O/O formalin. Temperature, salinity, dis- The RI1 index has been used by Gracia & Lozano solved oxygen, depth, and transparency (Secchi depth) (1980), Lara-Dominguez et al. (1981),Mallard Colmen- were measured at each collection. Observations of the ero et al. (1982), Chavance et al. (1984), Yaiiez-Aran- submerged and surrounding vegetation, benthic mac- cibia et al. (1985, 1986), Aguirre-Leon & Yanez-Aran- rofauna, tides and climatic conditions were made. cibia (1986). Study material. Sampling ylelded a total of 1200 Arius felis, 4511 Arius melanopus, and 113 Bagre marinus with a range of 35 to 337 mm, 25 to 282 and 70 RESULTS AND DISCUSSION to 240 mm total length (TL), respectively. A reference collection in the Ichthyology and Estuarine Ecology Abundance in relation to environmental parameters Laboratory at the Institute of Marine Sciences and Limnology, Mexico was used: catalogue reference Arius feliswas captured in a salinity range from 0 to CCML-PF 0.001562/1568 (Camp.) for A. felis, CCML- 37 %o (Fig. 2), temperature from 21.5 to 32 "C, and PF 0.001569/1573 (Camp.) for A. melanopus, and water transparency from 0.3 to 2.1 m. Its abundance CCML-PF 0.001556/1561 (Camp.) for B. mannus. was positively related to salinity (r = 0.86). Abundance, size, food and feeding habits, sex and gonadic maturity as a function of time and space were Arius felis determined as described in Nikolsky (1963), Randall (1968), Yanez-Arancibia et al. (1976, 1986), Hyslop (1980), Lara-Dominguez et al. (1981), Chavance et al. 5 0 20 30 12 (1984, 1986), Sanchez-Gil & Yanez-Arancibia (1985). .S;i The Relative Importance Index (RII) of Yanez-Aran- W '0 cibia et al. (1976), was employed to quantify the rela- I? tive importance of any trophic group (= items). This approach takes into consideration the frequency of occurrence and the weight of the food in the gut:

where RI1 = Relative Importance Index; F = frequency of occurrence for each food item expressed as a percentage; G = gravimetric percentage of each item. The RI1 index is expressed as a percentage with a natural range of zero to 100. (The abundance of each item as a parameter is not used because it erroneously gives the same importance to small and large organisms.) The RI1 2.5 7.5 12.5 17.522.52:.532.537.5 index then is combined with the frequency of occur- SALINITY ('loo) rence and the weight of food items into a trophic dia- Fig 2 Arjus mclanopus, A felisand Bagre marinus. Percent- gram (see for example Fig. 8 on food). This dlagram age of b~omass(g m ') In relation to salinity. Also shown is represents the spectrum of food of one species, which is cumulated percentage of biomass related to salinity Yafiez-Arancibia & Lara-Dominguez. Ecology of three sea catfishes 219

Arius melanopus was captured over a salinity range ranged from 140.5 to 219.4 mm (TL); the entire popula- of 0 to 36 %O (Fig. 2), temperatures from 20 to 32 "C, and tion averaged 160.1 mm, indicating that Terminos water transparency from 0.3 to 1.2 m. The abundance Lagoon is dominated by juvenile and subadult A. felis. of this species was negatively correlated with salinity In general, smaller sizes were found during the end of (r = -0.90). A. melanopus exhibited 2 peaks of abun- the rainy and beginning of the nortes season (October dance in relation to salinity, the first related to juveniles and November), while the largest individuals were living at low salinity (< 5 %o),and the second the result present during the end of the nortes and beginning of of capture of adults living at salinities from 25 to 35 %o. the dry season (December and February) (Fig. 3C). Bagre marinus was captured in a salinity range from There were 2 biomass peaks for A. felis in June and

4 to 32 %O (Fig. 2), temperatures from 22 to 31.5 "C and November (Fig. 3B). The November peak corre- water transparency from 0.2 to 1.6 m. This species was sponded to a peak in density, but the June peak did not evenly distributed with respect to salinity. (Fig. 3A). This is because the November biomass peak was due to the presence of a high number of juveniles, but the June biomass peak was due to fewer, but larger Seasonal variation adults. Arius melanopus also occurs throughout the year in Arius felis occurs throughout the year in the lagoon. the lagoon. Catches of individuals ranged from 24 in The number of individuals varied from 8 in April 1981 March 1980 to 420 in August 1980 (Table 3; Fig. 3A). to 144 in November 1980, with density fluctuating in Density varied from 0.0007 in March to 0.0134 ind. m-' the same way from 0.0003 to 0.0046 ind. m-2, respec- in August 1980. Maximum biomass (0.52 g m-2) was tively (Fig. 3A). Biomass ranged from 0.0201 in April recorded in March 1981 (Fig. 3B). Average TL ranged 1981 to 0.2076 g m-2 in November 1980 (Table 2; between 80.0 mm in August and 186.6 mm in July Fig. 3B). The average size of individuals collected 1980. Generally, the population of A. rnelanopus was dominated by small individuals from the end of the fr, i- rAr~usfells rainy season through the nortes season (from August to : , *-----Ar~usmelanopus a f o-....oBagre rnarlnus January), while large sizes were dominant from the end of the nortes season through the dry season (from February to July) (Fig. 3C). These data suggest that Terminos Lagoon serves as a nursery area for A. melanopus. Bagre marinus was collected in trawls primarily from June 1980 to January 1981 and also in April 1981 (Table 4; Fig. 3).The greatestnumber of individuals (31), highest density (0.0012 ind. m-') and greatest biomass (0.0157 g m-') occurred in November 1980 (Fig. 3A, B). Average TL ranged from 80.5 mm in July 1980 to 125.9 mm in January 1981. Generally only juveniles were collected in the lagoon (Table 4; Fig. 3C).

Spatial variation

- 220. * c Arius felis was widely distributed throughout the 5 major habitat types in Terminos Lagoon (Figs. 1 and 4). However, it was most common in the inner littoral area 2. of Carmen Island (Stns 6, 7, 12, 13, 18, and ESP) and \ I \I t 2 140. b 1 G: Puerto Real Inlet (PRI) (Table 2; Fig. 4). This species 2. I, '' D 120. I'I ' was also common among communities of the inner Y. 19 .....o; ,..0 ..0.'' ,''.o" shelf in the Southern Gulf of Mexico. Although A, felis 2 100. ,.: . . U. 0. . .:,L ...... L,- . . has a broad distribution on the inner shelf, 68 O/O of this P 807, , , , , , MAMJJ AS0tJDJFLIA population is reported to be in the western portion of 1980-C 1981 MONTHS Campeche Sound in a typical marine habitat (Yafiez- Arancibia & Sanchez-Gil 1986). In Terminos Lagoon Fig. 3. Arius felis, A. rnelanopus and Bagre rnarinus. Seasonal patterns in numbers of individuals, biomass (g m-2) and aver- the greatest biomass (0.198 g m-2) and highest fre- age total length (mm) quency of occurrence (59 %) occurred in areas with a Table 2. Arr~rsfelis. Nuniber (N) and weight (W; g) of sea catfish caught during a 12 rnin haul of each station and during each month. Only stations where this species were collected are shown

Slations Totals Density (to-' ind m-') Biomass Mcrnth I 2 3 4 .i B 7 8 9 10 11 12 13 14 15 16 17 18 (10 ' 11 IT-') PRI" ESP"

Mar 80 N 0 0 I H 1 0 11 6050 3 13 1041 8 89 0.26 - W 0 0 176.2 432.4 180.5 0 651 0 243.5 0 186.3 0 420.0 154.7 24.4 83.9 0 355.8 936.9 3845.6 1.142 - Apr R0 N 0 1 0302320001 2210001853 0.16 0 14(j.5 0 192.4 0 1665.7 123.4 0 0 0 8.2 226.9 217.1 7.0 0 0 0 593.6 3180.8 0.964 - - Mdy 80 N 0 0 0 0 0 501000581400000 0 87 0.28 - 2 W 0 0 0 0 0 247.4 0 399.3 0 0 898.5 1462.4 0 0 0 0 0 0 3007.6 0.955 - 63.7 Jun 80 N 9 0 1 3 6 000110 0 10 0 026 32 80 0.24 5

W 37 0 0 126.7 276.0 638.2 O 0 0 4 1.8 53.4 0 0 167.6 0 0 0 712.7 4903.1 6956.5 2.066 858.7 - Jul 80 N 0 0 0 17 6 300030 00315024 62 0.16 2 51 W 0 0 0 222 0 86.4 58.9 0 0 0 298.3 0 0 0 222.3 73 0 106.0 0 2190.9 3265 8 0.852 141.1 1434 6 Aug 80 N 0 L 094 000010 131066 3 35 0.11 10 M1 0 99 0 l35 0 73.7 0 0 0 0 25.4 0 198.6 317.7 8.1 0 319 5 81.2 344.3 1603.4 0.510 431.3 - Svp 80 N 0 1 0 0 12 200000 0117021 3 39 0.12 - 102 W 0 (5.1 0 0 504.4 448.3 0 0 0 O 0 0 1504.4 153.4 0 98.8 128.1 369.8 3213.3 1.004 - 3190.8 OcL 80 N 19 .3 4 0 16 0010104011010 4 64 0.20 44

W291.8 135.0 739.4 0 540.1 0 0 197.1 0 27.9 0 467.0 0 26.7 809.2 36.5 0 363.9 3634.6 1.154 1854.4 - Nov 80 N 0 0 1 062 18 012 0 4 1 2 3 7 8 0 14 12 144 0.46 - 7 W 0 0 157.3 0 891.2 1719.7 0 813.3 0 242.9 21.9 284.2 357.6 175.7 402.2 0 223.7 1201.3 6491.0 2.076 - 158.3 Der R0 N 0 0 2 1 2 400000 1110005 1 27 0.08 59 - W 0 0 2329 38.8 168.4 674.7 0 0 0 0 0 14481586.8 0 0 0 22.0 32.7 2901.1 0.879 8411.8 - Jal181N 0 7 0 1 27 100000 3906131 3 71 0.22 - 21 CV 0 157 2 0 38 2 585.0 243.2 0 0 0 0 0 417 1 1486.5 0 514.7 518 1 77.9 164.0 4201.9 1.313 - 1278.6 Feb81NO I 0 O 0 200000 000312 2 10 0.03 10 38 WO 0 0 0 0414.70 0 0 0 0 0 0 0 407.8 255.1 96.7 165.7 1340.0 0.423 787.7 2278.5 MarHINO 0 0 2 b 100000000168411 48 0.15 - - W 0 0 0 250.8 579.5 337.5 0 0 0 0 0 0 0 0 346.6580.6 43.8 269.6 2408.4 0.777 - -

Ap81N 0 O 0 0 2 000000010000 5 8 0.03 33 p \.V 0 0 0 0 3046 0 0 0 0 0 0 0 42.0 0 0 0 0 295.9 642.5 0.201 2959.9 - Toldl N 28 13 9 44 144 59 13 29 1 15 60 30 42 23 45 36 100 126 817 l63 221 L\] 328.8 5447 1432.5 1585.6 4552.0 5810.1 774.4 1653.2 41.8 834.2 928.6 3621 0 5834.4 617.6 2637.4 1914 6 1741.9 11839.7 46692.5 15444.9 8404.5

" PR1 = Pue~toResl Inlcl (for d~slr~huliol~In Fig. 4) ' ESP - Eslcro Pargo Inlel (for dislrlb~~llonIn Fig. 4) Table 3. Arius rnelanopus. Number (N) and weight (W; g) of sea catfish caught during a 12 rnin haul of each station and during each month. Only stations where this species were collecled are shown

Stations Totals Density (10-' ind m-') B~orn~~ss Month 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 (10.' g m-') PRI" ESPt'

Mar 80 N 0 0 l 5 0 051 5 1 00400 0 2 0 24 0.07 - - W 0 0 41.6 61.3 0 0 385.4 67.6 105.5 8.8 0 0 413.6 0 0 0 44.0 0 1127.8 0.335 - Apr 80 N 0 0 34 29 0 400 1 0 20227 1 0 0 40 140 0.42 - W 0 0 2150.0 2125.6 0 282.5 0 0 79.3 0 117.2 0 347.1 334.7 89.1 0 0 2309.9 7835.4 2.374 - - May 80 N 0 0 0 17 0 500 0 030100 8 2 0 0 63 0.20 - - W 0 0 0 273.1 0 237.7 0 0 0 0 1458.7 109.0 0 0 296.8 85.4 0 0 2460 7 0.781 - - Jun 80 N 0 41 18 51 9 000 4 2 00000 1 0 1 127 0.38 - - W 0 343.3 981.6 1940.3 740.5 0 0 0 176.0 62.6 0 0 0 0 0 72.9 0 39.4 4356.6 1.294 - - Jut 80 N 0 12 8 13 0 000 1 0 0302 0 3 0 3 45 0.12 - l M' 0 767.9 286.4 559.3 0 0 0 0 55.6 0 0 523.2 0 48.6 0 143.6 0 355.8 2740 4 0.715 - 95 4 Aug 80 N 65 6 31 232 0 00028 1 1002 0 24 27 3 420 l 34 8 - W 49.9 130.0 1218.5 629.2 0 0 0 0 717.2 23.5 31.4 0 0 130.3 0 633.21154.3 133.5 4851.0 1.544 366.5 - Sep 80 N 94 100 0 144 2 000 5 10 0000 1 1 12 0 369 1.15 - W 59.1 1798.2 0 2977.8 216.3 0 0 0 111.8 332.4 0 0 0 0 61.4 25.8 582.1 0 6164.9 1.927 - Oct R0 N 0 21 58 34 0 000 3 1 7000 1 5 0 0 130 0.4 1 232 - W 0 522.9 1400.2 1186.2 0 0 0 0 64.6 168.3 313.4 0 0 0 37.6 2833 0 0 4976 5 1.580 17730.8 - Nov 80 N 12 33 83 7 0 301 2 28 1010 9 61 13 0 254 0.81 - 4 W 113.6 384.5 2764.1 258.5 0 335.2 0 52.8 109.7 1010.2 57.8 0 1.0 0 505.8 1562.1 726.7 0 7882.0 2.516 - 301.4 Dec 80 N 0 0 12 17 1 100 0 1 0000 0 0 3 46 81 0.25 12 - W 0 0 807.9 501.8 137.7 79.6 0 0 0 49.5 0 0 0 0 0 0 239.0 1822.3 3637.8 1.102 874.6 - Jan 81 N 6 21 157 30 12 000 1 10 00002635 3 0 301 0.94 - 73 W 68.3 42.5 5608.8 53.8 512.5 0 0 0 2.2 532.6 0 0 0 0 1134.6 1739.9 164 5 0 9859.7 3.081 - 4622 3 Feb 81 N 0 0 73 0 0 000 0 0 00000 0 1 2 76 0.24 - 70 W 0 0 2657.3 0 0 000 0 00000 0 0 35.6 96.6 2789.5 0.881 - 3695.0 Mar 81 N 0 0 45 3 0 180 0 0 1 0 00005 0 9 56 299 0.96 - - W 0 0 2550.3 221.0 0 10217.3 0 0 145.7 0 0 0 0 0 74.3 0 354.8 2718.4 16281.8 5.252 - - Apr 81 N 0 1 5 29 02400 4 1 002015 6 0 7 94 0.29 - - W 0 90.2 224.1 911.7 0 2551.2 0 0 138.8 36 0 0 0 214.4 0 772.9 383.1 0 503.6 5826.0 1.821 - - Total NI77 235 525 611 24 217 5 2 55 55 41 4 9 31 66 138 70 158 2423 253 148 W 290.9 4079.4 21690.8 11699.6 1607.0 13703.5 385.4 120.4 1706.4 2223.9 1978.5 632.2 976.1 513.6 2972.5 4929.3 3301.0 7979.5 80790.1 18552.4 8714.1

" PR1 - Puerlo Real lnlet (for d~stributionin Fig. 5) "ESP = Estero Pargo lnlet ([or dislribulion m Fig. 5) 1 222 Mar. Ecol. Prog. Ser 49: 215-230, 1988

Table 4. Bagre marinus. Number (N)and we~ght(W; g) of sea catfish caught during a 12 min haul of each station and during each month. Only stations where this species were collected are shown

Stations Totals Density (10-~ind Biomass Month 1 2 4 5 8 9 10 11 14 15 16 17 (10-l g m-2)

Jun 80 N 3 10 0 0 00000 0 0 0 13 0.04 W 18.8 58.3 0 0 000000 0 0 77.1 0.023 Jul 80 N 0 1 1 0 00000 0 0 0 2 0.01 WO 5.3 7.4 0 00000 0 0 0 12.7 0.003 Aug 80 N 9 2 1 0 00602 0 0 0 20 0.06 W 65.6 19.4 5.7 0 0 0 90.7 0 30.8 0 0 0 212.2 0.068 Sep 80 N 8 7 4 0 01000 0 1 0 21 0.07 W 49.6 36.6 77.1 0 0 4.8 0 0 0 0 196.4 0 364.5 0.114 Oct 80 N 2 2 4 0 00010 0 0 0 9 0.03 W 13.7 14.8 22.0 0 0 0 0 4.4 0 0 0 0 54.9 0.017 Nov 80 N 15 8 6 2 2 0 0 0 0 1 0 4 38 0.12 W 161.3 57.3 61.3 23.2 19.5 0 0 0 0 17.0 0 152.7 492.3 0.157 Dec 80 N 0 1 0 0 00000 0 0 0 1 0.003 W 0 10.3 0 0 00000 0 0 0 10.3 0.003 Jan81N 3 2 0 2 00000 0 1 0 8 0.03 W 50.2 45.4 0 27.8 0 0 0 0 0 0 19.3 0 142.7 0.045 Apr81N 0 0 0 0 010000 0 0 1 0.003 W 0 0 0 0 0 33.8 0 0 0 0 0 0 33.8 0.01 1 Total 40 33 16 4 2261 2 1 2 4 113 359.2 247.4 173.5 51.0 19.5 38.6 90.7 4.4 30.8 17.0 215.7 152.7 1400.5 persistent marine influence and dominated by seagrass Island (Stns 6, 7, 12, and 13). The largest size classes, meadows (Figs. 1 and 4). The population of A. fells was although present throughout the lagoon, were most made up of juveniles as well as adults 35 to 377 mm TL prevalent in the inner littoral region of Carmen Island (Fig. 4). Small individuals occurred mainly in the cen- (Fig. 4). tral basin (Stns 8, 11, 14, and l?), the eastern portion of Arius melanopus was also widely distributed in all the fluvial-lagoonal system (Stns 10, 15, and 16) and in habitats in Terminos Lagoon (Figs. 1 and 5). How- Carmen Inlet (Stns 1,2, and 5). Intermediate size ever, the highest values in biomass (0.392 g m-2), classes were found in the inner littoral areas of Carmen density (0.0199 ind. m-') and frequency of occurrence

Arius felis

Fig. 4. .Mus felis. Spatial distribution showing size class structure for each collection station during the sampling period. N: number of fish; TL: total average length; Fr: frequency Yanez-Arancibia & Lara-Dominguez: Ecology of three sea catfishes 223

Arius melanopus

Fig. 5. Anus melanopus. Spa- tial distribution showing size class structure for each collection station during the sampling period. N: number LDV)~LDLOY)V) U)LOV)V)LDU)uY LOLOV)V)LOV)V) V)LOV)LO!nV)LD of fish; TL: total average O"-zzgk Dh=y)cc9I; O-:zO)z& O-=V)O)zk length; Fr: frequency TOTAL LENGTH (mm)

(86 %) were found near areas of river discharge, the inner Littoral areas of Carmen Island (Stns 6, 7, especially in the southwestern and western portions 12, and 13) (Fig. 5). of the lagoon (Fig. 5). The population structure of A. Bagre marinus was collected mainly in Carmen Inlet, rnelanopus in Terminos Lagoon consists of small and and to a lesser degree in the central basin and areas of large fish ranging from 25 to 282 mm TL, (X = freshwater influence (Figs. 1 and 6). This is a common 132.7 mm TL) (Fig. 5). Small individuals were found species in communities of the inner shelf in the South- mainly in Carmen Inlet (Stns 1 and 2) and in the ern Gulf of Mexico with a broad distribution; neverthe- western portion of the fluvial-lagoonal systems (Stns less, over 80 O/O of this coastal population is found in the 4 and 9). Intermediate size classes were found in the western portion of Campeche Sound in areas highly central basin of the lagoon (Stns 11, 14, and l?), in influenced by land run-off (Yafiez-Arancibia & San- the western portion of the fluvial-lagoonal systems chez-Gil 1986). In Terminos Lagoon, the greatest bio- (Stns 10, 15, and 16) as well as the interior of the mass (0.008 g m-'), density (0.0009 ind. m-2), and fre- Palizada-del Este fluvial-lagoon system (Stn 3), and quency of occurrence (38 %) were in Carmen Inlet the northeast portion of the lagoon (Stn 18). Large which is a highly variable portion of the system fish were found throughout the lagoon, but mainly in (Table l). The B. rnannus population consisted of

Bagre marinus 0>0.92~10-~ ~<0.72~10-~

Fig. 6. Bagre marinus. Spatial distribution showing size class structure for each collection station during the sampling ~eriod.N: number of fish: TL. total average length; Fr: frequency TOTAL LENGTH (mm) 224 Mar Ecol. Prog. Ser. 49: 215-230, 1988

juveniles 79 to 240 mm TL (X= 107 mm TL) (Fig. 6). September (rainy season). It takes place in the inner Small individuals occurred in the Carmen Inlet area littoral area of Carmen Inlet mainly in Estero Pargo (Stns 1, 2, and 5) (Fig. 6), while larger fish were preva- Inlet (ESP), in the northwest portion of the lagoon, and lent in the eastern portion of the fluvial-lagoon system in the eastern sector of the adjacent continental shelf (Stns 10, 15, and 16). (Yanez-Arancibia & Sanchez-Gil 1986). Spawning

takes place at an average salinity of 24.8 %Q, an average temperature of 30.3 "C and average transparency of Maturity and seasonal reproduction 49 "h, in depths not exceeding 3.5 m. Arius melanopus. All maturation stages also were Ariusfelis. All the gonadal maturity phases proposed observed for this species. Individuals in Phases I, 11, and by Nikolsky (1963) were noted. Individuals in Phases I, 11, V11 were present throughout the year, while individuals and V11 were present in our collections throughout the in Phase I11 of gonadal maturation were collected year. The greatest quantity of Phase 111 occurred in June, mainly from April to September. Those in Phase IV while Phase IV was only present from June to September. were only found from April to September and spawn- Individuals in Phase V1 were caught from August to ing adults (Phase VI) were recorded only from March December (Fig. 7). The minimum size where a Phase 111 1980 to January 1981 (Fig. 7). gonadal stage (in maturation) was found was 186 mm TL. The minimum size at which females reached Phase Data on maturation stage (Phase 111, IV, and VI) in relation 111 (in maturation) was determined to be 144 mm TL. to fish length were analyzed in order to determine at what Data on maturation stage (Phases 111, IV, and VI) in length 50 % of females are expected to mature. These relation to fish length were analyzed in order to deter- analyses indicated that length at first maturity is 250 mm mine at what length 50 % of females are expected to TL. Males were caught during August and September, in mature; it appears that length at first maturation is Estero Pargo Inlet (ESP) as well as near Puerto Real Inlet 187 mm TL. Males from 163 to 211 mm TL with eggs (Stn 18), measuring from 236 to 307 mm TL with eggs and/or embryos in their mouths were captured from and/or embryos in the mouth. June to September in the western portion of the fluvial- The breeding season of Anus felis is from June to lagoonal system (Stns 3, 4, and 9).

Armmelonopus

Ar~usfelis m- PHASE 1 iqI?:?'JL, v, 10 20- PHASE11

10 - PHASE I1 20 N.742 10- W%-

PHASE IV N=75 10 G C PHASE VI

, , L ,l, , , , f , -, , PHASE VII ;:W1,, 20- N.149 lo-[-? >'L+ 10 U- MAMJJASONDJFMA MAMJJASONDJFMA 1980+ 1981 1980+ 1981 MONTHS MONTHS

Fig. 7. Anusfeljs and A, melanopus. Monthly rnaturat~onstage for both males and females in Terminos Lagoon Yanez-Arancibla& Lara-Domingue,z. Ecology of three sea catfishes 225

The breeding season for Arius melanopus is from Bagre marinus. This species is a second order and April to September (near the end of the dry to rainy occasionally third order consumer with a diet com- seasons), and takes place in areas of persistent fluvial posed of a least 12 types of food (Table 5).According to influence, mai.nly towards the western portion of the the index of Yanez-Arancibia et al. (1976), the main fluvial-lagoon system. Salinity averaged 21 '%0, tern- food of juveniles is unidentifiable organic matter peratures 29.4 "C, and transparency averaged 37 % in (MOND);the secondary food is made up of fishes, with depths not exceeding 3.5 m. smaller amounts from other trophic groups (Fig. 8). Bagre marinus. Only Phases I and I1 of the gonadal maturity stages were observed for this species. The greatest abundance (34)of individuals in Phase I occur- Ecological synthesis and conceptual models red in November 1980. Gunter (1945) and Pew (1971) established that the spawning of this species takes Arius felis. This species migrates continuously place near the shoreline in shallow areas, and Gunter between the lagoon and the adjacent inner shelf (1945) reported 70 d as the oral gestation period in throughout the year. Apparently, there are 2 principal Texas, USA. Spawning presumably occurs on the adja- inmigrations from the sea. The first occurs between cent continental shelf at depths lesser than 20 m during ~Llarchand June (principally in May), and consists of April to June (dry season) (Yafiez-Arancibia & San- adults which colonize shallow, protected spawning chez-Gil 1986).Therefore juveniles of ages from ca 2 to areas. The second, between September and November 4 mo appear to recruit to the lagoon from June to (principally November), consists of juveniles which November during the rainy and nortes seasons. Similar have migrated to the lagoon from the Puerto Real Inlet observations have been made by Lara-Dominguez & and the inner western shelf areas. Yanez-Arancibia (1986) and Yafiez-Arancibia & San- Based on the data we have presented on distribution, chez-G11 (1986). feeding, and life history stage, we have developed a conceptual model of the ecological interactions of Arius felis (Fig. 9). Towards the end of the dry season and the Food and feeding habits beginning of the rainy season ('1' in the diagram in Fig. 9, upper left) there are sexually mature adults Arius felis. Adults ingested a broad spectrum of food present in the coastal environment. These adults (Table 5) comprised of at least 16 categones (items). migrate from deeper water towards shallow, protected According to the index of Yafiez-Arancibia et al. (1976), areas of the eastern section of the adjacent continental adults greater than 200 mm TL feed primarily on shelf and enter Terminos Lagoon through Puerto Real unidentified organic matter; the secondary food is crus- Inlet, and move to the inner littoral areas of Carmen taceans, fishes, and blue crabs; and circumstantial Island and the eastern portion of the lagoon (Estero foods make up other trophic groups (Fig. 8). As noted Sabancuy), based on our observations of juvenile dis- previously, this method of assessment combines infor- tribution and gonadal index. These locations are used mation on weight of food items, frequency of occur- for reproduction and nursery areas. During the nortes rence and the RII. season ('2' in Fig. 9, upper left), juveniles and postre- Arius felis is predominantly a second order consumer productive adults leave the spawning areas, cross the feeding on detritus, meio- and macrobenthic fauna, central basin of the lagoon and move to Carmen Inlet and fishes, and occasionally is a third order consumer. where they migrate, mainly to the adjacent continental The diet changed with size and locality; luveniles (less shelf, or sometimes towards the other ecological sub- than 200 mm TL) prey on small crustaceans such as systems within Terminos Lagoon. Marshes and areas of amphipods, shrimp, blue crabs, mollusks, and annelids freshwater influence in the lagoon and the shelf are (Table 5), while the greater proportion of the adults' feeding areas for adults; gonadal maturation of food are large prey such as fish (Table 5; Fig. 8). juvenile preadults take place during the dry season ('3' Arius melanopus. Adults of this species also ingest a in upper left of Fig. 9). broad spectrum of food (Table 5) composed of at least Finally, maturing adults leave the feeding areas for 16 food categories. According to the index of Yaliez- breeding and nursery areas. The migration of Arius Arancibia et al. (1976) the main food of ad.ults felis in Terminos Lagoon generally follows the prevail- (> 160 mm TL) is unidentifiable organic matter ing east-west current pattern. Seasonally, the migra- (MOND). The secondary food is comprised primarily of tion is influenced by high salinity conditions in inner crustaceans and mollusks. This species is predomi- littoral areas of Carmen Island and the northern lagoon nantly a second order consumer omnivore in Terminos during the reproduction period; juveniles are princi- Lagoon and there are no diet differences with size pally associated with low salinlty areas. (Table 5; Fig. 8). Arius melanopus. Compared to Arius felis, A. Tablc 5. Stomach contents of the 3 sea catfish specles in Ternunos Lagoon. N: percentage by number; G: percentage by weight; F: percentage by frequency oI occurrence; NI: Relative Importance Index

Adults > 200 mm TL Juveniles < 200 mm TL Adults :. 160 mm TL Juveniles < 160 mm TL (N .- 50) (N = 30) (N: 77) (N = 39) N G F R11 N G F RI1 (X) (%) (%l (%) ("A) (%)

Foram~nilers(Fo) Nenlatomorphes (Ne) Ech~nodern.~~(Eq) Acantocephalus (Ac) h,lollusks (MO) Annelids (Ane) Copcpods (CO) Ostracods (OS) Curnaceans (Cu) Amphipods (An) Tanaiddc~d(Td) Isopods (Is) Penartrs sp. (Pe) Palaemon~ds(Pa) Blue crabs (Ca/.l) Euphausilds (Eu) C:rustaceans renrdlns (RC) Eggs/larvae of ~r~vcrlcbrales(LI) Fish remains (RF) Vegetal debris ([(V) Sed~rnenls(Sd) Indeterminate orgdnic nidller (MOND) Yanez-Arancibia & Lara-Dominguez: Ecology of three sea catfishes 227

DRY SEASON cs Arius felk 1

RAINY SEASON

"NORTES" SEASON

Arius melanopus Eno ADULTS TOTAL N=77 111

Fig. 9. Anus felis. Conceptual model of ecological cycle in Terminos Lagoon. It illustrates the migratory patterns of adults (A) and juveniles (J) as adaptations to their reproductive and feeding strategies from the northeastern sector of the lagoon (ECI; El Carmen Island) and the eastern portion of the adja- Bagre marinus cent continental shelf (CS) toward the central basin of the 80 TOTAL N=37 lagoon (CB) and areas of freshwater influence (fluvial- 70 lagoonal system; FLS). Cycle in the upper portion shows the ! behaviour with respect to the climatic period and related to salinity (S),temperature (T) and depth (D)gradients: see text for explanation

Fig. 8. Anus felis, A. melanopus and Bagre marinus. Com- bined trophic diagram showing the trophic spectrum of adult populations of A. fells (> 200mm TL), A. melanopus (> 160 mm TL) and juvenile population of B. marinus in Ter- minos Lagoon. Abbreviations and data of the diagram are indicated in Table 5 melanopus is a typically estuarine species, completing its entire life cycle in Terminos Lagoon. This species is one of the most abundant sea catfishes in terms of number and biomass, and is one of the best adapted both morphologically and physiologically to the lagoon-estuarine system (Yaiiez-Arancibia et al. 1980). The data suggest that the species carries out migrations within the lagoon for reproductive and feeding pur- Fig. 10. Anus melanopus. Conceptual model of ecological poses. cycle in Terminos Lagoon. It illustrates the migratory patterns A conceptual model for Anus melanopus, based on of adults (A) and juveniles (J) as adaptations to their reproduc- data presented above, is shown in Fig. 10. At the end of tive and feeding strategies from the fluvial-lagoonal system the dry season and beginning of the rainy season ('1' in (FLS) toward the central basin of the lagoon (CB) and the inner littoral of Carmen Island (ECI). Cycle in the upper Fig. 10, upper left) the fluvial-lagoonal system (mainly portion shows the behaviour with respect to the climatic in the western section) serves as the primary spawning period and related to salinity (S), temperature (T) and turbidity and main nursery area. At the end of the rainy season (Tu) gradients: see text for explanation 228 Mar. Ecol. Prog. Ser. 49: 215-230. 1988

and the beginning of the nortes season ('2' in Fig. 10, season ('2' in Fig. 11 upper left), juveniles leave the upper left), juveniles and postreproductive adults leave mouths of adult males and remain in the shallower the spawning areas and move to the central basin of the protected areas of the shelf, or enter Terminos Lagoon lagoon. At the end of the nortes season and the begin- through Carmen Inlet where they feed and grow. Post- ning of the dry season ('3' in Fig. 10, upper left), the reproductive adults at this time of the year move to inner littoral areas of Carmen Island are feeding zones deeper water of the shelf. At the end of the nortes for both adults and preadults. Finally, maturing adults season ('3' in Fig. 11, upper left), juveniles leave the leave the inner littoral areas of Carmen Island and lagoon through Carmen Inlet, moving toward deeper return to the spawning areas. Salinity, temperature and areas, where they continue growing and reach gonadal turbidity gradients seem to be the most important fac- maturity. The migrabon pattern of B. mannus is princi- tors related to the proposed model (Fig. 10). Based on pally associated with juvenile and preadult feeding analysis of distribution trends, reproductive movement strategies. The species immigrates to Terminos Lagoon is in the same direction as the prevailing currents through Carmen Inlet against the current pattern, from whereas the feeding movement is against the current. greater to lesser depths, transparency and salinity, but Bagre marinus. This is mainly a marine species, from lesser to higher temperatures. Migration from the typical of the demersal fish communities of the adja- lagoon to the sea occurs through the same passage cent continental shelf (Yariez-Arancibia et al. 1985, following the prevailing water movement. Yafiez-Arancibia & Sanchez-Gil 1986). Apparently, B. marinus enters Terminos Lagoon and is a cyclical component of the fish community of this ecological CONCLUSIONS system since it is only present during the rainy and nortes seasons. It carries out important stages of its life The partitioning of spawning areas in different cycle in the lagoon-estuarine environment such as habitats within Terminos Lagoon illustrates that the 3 feeding and nursery. sea catfishes are capable of colonizing most lagoon A conceptual model for Bagre marinus is illustrated habitats and utilize a trophic spectrum width peculiar in Fig. 11. At the beginning of the rainy season ('l' in to each species. Such adaptative strategies are very Fig. 11, upper left), the species reproduces in shallow advantageous in inter- and intra-specific competition. waters of the western sector of the adjacent continental As an example, Arjus melanopus breeds in the south- shelf. This zone also serves as a nursery area. At the ern fluvial-lagoon systems and wetlands associated end of the rainy season and the beginning of the nortes with Terminos Lagoon, A. Eelis spawns in the northern seagrass meadows areas including Puerto Real Inlet and the adjacent inner shelf, whereas Bagre mannus Bagre marinus breeds in the inner shelf adjacent to Carmen Inlet. In tropical latitudes the biological patterns are

RAINY SEASON directly related to high productivity in coastal waters, large supply of organic matter, increased food availability, and protection from predators. Because of this, estuary-sea or swamp-estuary fish migrations may be interpreted as small-scale anadromous adaptations. This is an important viewpoint when considering future sea catfish aquaculture.

Acknowledgemenfs.We thank the Institute of Marine Science and hmnology, UNAM, for its institutional and financial support for this research. This research is part of the following projects. Ecology, Use, Resources and Management of Coastal Ecosystem in the State of Campeche PCECBNA-021924; 91'20' Estuarine-Shelf Interactions in the Region of Terminos Lagoon Fig. 11. Bagre marinus. Conceptual model of ecological cycle PCECBNA-021925, sponsored by CONACYT, Mexico and in Terminos Lagoon. It illustrates the migratory patterns of UNAM; and part of the project Bioecology of the Mangrove adults (A) and juveniles (J) as adaptations to thelr reproduc- System In Mexico, Southern Gulf of Mexico (05-87-52B-361- tive and feeding strategies from the western portion of the ME1) sponsored by the Organization of American States adjacent cont~nentalsh.elf (CS) toward t.he central basin of the (OAS),CONACYT. Mexico and UNAM. We acknowledge the lagoon (CB) and areas of freshwater influence (FLS) through help of Margarita Caso-Chavez in processing some of the fish Carmen Inlet (Cl). The cycle in the upper portion shows the collection; Eduardo Sainz Hernandez for processing of data behaviour with respect to climatic penod and temperature (T) and computing results, and Patricia Sanchez-Gil for help in and depth (D) gradients: see text for explanation coordination of laboratory work. Part of this manuscript was Yanez-Aranclbla & Lara-Doming uez. Ecology of three sea catfishes 229

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This article was presented by Dr G. W. Thayer; it was accepted for prinbng on August 25, 1988