Distribution and Abundance of Four Caiman Species (Crocodylia: Alligatoridae) in Jaú National Park, Amazonas, Brazil*

Home , Alligatoridae, Alligatorinae, Black Caiman, Caiman, Caiman (genus), Paleosuchus

Rev. Biol. Trop. 49(3-4): 1095-1109, 2001 www.ucr.ac.cr www.ots.ac.cr www.ots.duke.edu

Distribution and abundance of four caiman species (Crocodylia: Alligatoridae) in Jaú National Park, Amazonas, Brazil*

George Henrique Rebêlo1 and Luciana Lugli2 1 Instituto Nacional de Pesquisas da Amazônia, Coordenação de Pesquisas em Ecologia, Caixa Postal 478, 69011-970 Manaus-AM, Brazil. Phone: 55 92 6431820. E-mail: [email protected] 2 Universidade Estadual Paulista, Rio Claro-SP, Brazil. Phone: 55 19 5332952. E-mail: [email protected]

* This study is dedicated to the memory of our friend, the Brazilian herpetologist and political activist Glória Moreira [1963-1997].

Received 17-I-2000. Corrected 03-X-2000. Accepted 08-II-2001.

Abstract: Jaú National Park is a large rain forest reserve that contains small populations of four caiman species. We sampled crocodilian populations during 30 surveys over a period of four years in five study areas. We found the mean abundance of caiman species to be very low (1.0 ± 0.5 caiman/km of shoreline), independent of habitat type (river, stream or lake) and season. While abundance was almost equal, the species’ composition varied in different waterbody and study areas. We analysed the structure similarity of this assemblage. Lake and river habitats were the most similar habitats, and inhabited by at least two species, mainly Caiman crocodilus and Melanosuchus niger. However, those species can also inhabit streams. Streams were the most dissimilar habitats studied and also had two other species: Paleosuchus trigonatus and P. palpebrosus. The structure of these assemblage does not suggest a pattern of species associated and separated by habitat. Trends in species relationships had a negative correlation with species of similar size, C. crocodilus and P. trigonatus, and an appar- ent complete exclusion of M. niger and P. trigonatus. Microhabitat analysis suggests a slender habitat partitioning: P. trigonatus was absent from river and lake Igapó (flooded forest), but frequent in stream Igapó. This species was the most terrestrial and found in microhabitats similar to C. crocodilus (shallow waters, slow current). Melanosuchus niger inhabits deep, fast moving waters in different study areas. Despite inhabiting the same waterbodies in many surveys, M. niger and C. crocodilus did not share the same microhabitats. Paleosuchus palpebrosus was observed only in running waters and never in stagnant lake habitats. Cluster analysis revealed three survey groups: two constitute a mosaic in floodplains, (a) a cluster with both M. niger and C. crocodilus, and another (b) with only C. crocodilus. A third cluster (c) included more species, and the presence of Paleosuchus species. There was no significant difference among wariness of caimans between disturbed and undisturbed localities. However, there was a clear trend to increase wariness during the course of consecutive surveys at four localities, suggesting that we, more than local inhabitants, had disturbed caimans. The factors that are limiting caiman populations can be independent of human exploitation. Currently in Amazonia, increased the pressure of hunting, habitat loss and habitat alteration, and there is no evidence of widespread recovery of caiman populations. In large reserves as Jaú without many disturbance, most caiman populations can be low density, suggesting that in blackwater environments their recovery from exploitation should be very slow.

Key words: Reptilia, Crocodylia, Amazonia, abundance, richness, wariness, Jaú National Park, Brazil.

Jaú National Park (JNP) is the world’s villages, and some are scattered throughout the largest rain forest reserve, located in Central area. Their staple foods are fish, turtles and Amazonia, in a nearly pristine condition. A manioc; their subsistence is supplied by prod- declining human population of a thousand peo- ucts that they extract to sell. Main products are ple inhabit the area and take its subsistence liana faggots, brazil nuts, copaíba oil, cassava from the forest. Most of them live in ten small flour, live turtles, aquarium fishes and timber 1096 REVISTA DE BIOLOGêA TROPICAL

(Guazelli et al. 1998). Water bodies are pre- Brazaitis et al. 1996b, Mohd Sah and Stuebing dominantly poor nutrient blackwater environ- 1996, Da Silveira et al. 1997). We examined ments that may affect plant richness and floris- the patterns of abundance and ecological rela- tic composition of the igapó (flooded forest) tionships among sympatric caimans in JNP, (Ferreira 1997). The rains are abundant and combining descriptive data with community the dry season short. As is common in other analysis techniques described by Ludwig and central Amazonia areas, the forest is flooded Reynolds (1988). during rainy season and the isolated pools dry We investigated specifically: (1) the up when rains are scarce (Richards 1996). caiman species abundances, diversity, and the The crocodilian assemblage is composed similarities between surveys, (2) the caiman of four Alligatoridae species (blunt head and species assemblage structure, (3) the human armoured crocodilians). Species interactions impact on caiman populations, (4) and the size- of amazonian crocodilians are poorly known age structures, which are important demograph- and studies examining patterns of that commu- ic parameters for conservation. nity have controversial conclusions (Medem 1971, Magnusson 1985). Two gregarious species inhabit quiet waters of great rivers and MATERIALS AND METHODS lakes: Melanosuchus niger (Spix, 1825) and Caiman crocodilus (Linnaeus, 1758). Studies Study area: The study was conducted discovered that Melanosuchus is absent from during 1993 and 1996 at Jaú National Park, sit- many areas of historic distribution, and this uated 200 km Northwest from Manaus, had been related to commercial hunting Amazonas State, Brazil (1º00’-3º00’S, 61º30’- (Medem 1971, 1981, 1983, Brazaitis et al. 64º00’W). In 1980, the Jaú River and its ripar- 1990, 1996a, b). ian areas up to the banks of the Unini and Two other species are the solitary, small, Carabinani rivers were established as a National and heavily armoured caimans of the genus Park (Act n¼ 85.200) to preserve their biological Paleosuchus Gray, 1862: Paleosuchus trigona- and cultural values. Because few rivers in tus (Schneider, 1801) observed in running Amazonia have this level of protection, the JNP waters and forest streams, and the dwarf P. provides an opportunity to study crocodilian palpebrosus (Cuvier, 1807) widely distributed assemblages and their habitat associations along throughout savannas and forests streams. a relatively undisturbed river. JNP has They are sympatric species in some localities, 22 720 km2. The climate is wet tropical but exclusive in other areas (Medem 1971, (Köppen Af), with rainy and dry seasons, the 1981, 1983). The thick bony plated skin of mean annual temperature ranges between 24-26 Paleosuchus is considered a successful adapta- ¡C, and the annual rainfall ranges between 1 tion to terrestrial life (Medem 1981); since it is 750 and 2 500 mm. Rainfall occurs throughout not suitable for tanning, commercial hunting the year, but the dry season is in July-November for this skin is low. and the wet season is in December-June. The We found a rather small caiman popula- annual variation of river level is near 7 m, and tion in JNP in a survey through different areas, the majority of the Igapó forest is flooded from habitats, and seasons. Crocodilian po-pula- 221 to 264 days each year (Anonymus 1998). tions of 1-10 individuals/km were more fre- The waters from the area have low conductivi- quently reported, while very dense populations ty, acid pH, low dissolved O2, and few suspend- (more than 10 individuals/km) were less fre- ed matter, with mean water temperature of 26.2 quently observed in different parts of the world °C (Díaz-Castro 1999). (see Glastra 1983, Montague 1983, Gorzula Sampling and data collection: The tran- and Paolillo 1986, Seijas 1986, Bayliss 1987, sects surveyed were selected within the JNP Gorzula and Seijas 1989, Espinosa 1995, study areas targeted by eight fieldteams INTERNATIONAL JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 1097 involved in the basic surveys to design the mm), and converted to scale. Caiman abun- management plan of the reserve. We per- dance was expressed as the number of animals formed nocturnal spotlight surveys, on open of each species (excluding hatchling pods) water, riverbanks and shoreline areas, using seen per kilometer. aluminium boats (6 m) equiped with 15-25 HP We identified the species in the field by outboard engines as the only platform. direct observation of morphologic characteristics We covered 231 km of the Jaú river and of at least three living animals: head shape, jaw tributaries in three areas and times: (i) Cutiaú pattern, and body color. The animal sizes (total (October 1993, March 1994, January 1996), lengths) were estimated at distances < 10 m. (ii) Central (July 1993, January and February Assemblage analysis: The impact of 1994), (iii) West (January 1996). We covered human presence was evaluated by comparison also 111 km of (iv) Rio Negro and the Jaú of the differences in the proportion of uniden- mouth (July and October 1993, April and tified caimans (eye proportion = wariness) September 1995), and 28 km of (v) the Unini between less and more disturbed areas and River and tributaries, in north JNP (September during survey series conducted in four locali- 1996). ties. Often, the animals fled before our To evaluate human impact we compared approach and were classified as eyes. These abundances between less and more disturbed constituted the main proportion of eyes report- areas. Less disturbed or rarely accessible to ed, but some eyes represented animals spoted non-dwellers, include all Jaú river areas (i, ii, inside inaccessible Igapó covering. We do not and iii), and more disturbed areas (with regular summed eyes to abundance of any other traffic of regional ships and most active trade species, as in other studies (e.g. Seijas 1988, of manufactured and extractive products) Da Silveira et al. 1997). The dominant species include the Jaú mouth, Rio Negro (iv) and can be different for different surveys, so we Unini river (v). chose to analyse eyes apart; too many eyes- We extensively searched the waters of JNP only observations may result in a common bias to find the caimans. Surveys were conducted at in crocodilian surveys (Bayliss 1987), but can night, begining 1 hr after sunset. Caimans were indicate the disturbance level of localities and located by eye-reflection using hi-powered wariness (Pacheco 1996, Ron et al. 1998). We spot-lights (powered by a 12 volts car battery). followed the suggestion of Ron et al. (1998) We moved slowly toward the animals to identi- that stated that an increase in the proportion of fy species, estimate sizes, and then captured a eyes reflects an increase in wariness and a sample of animals to correct for size estimates. behavioral response to human disturbance. A common sampling error is imprecise size esti- To examine habitat partitioning we identi- mates (Magnusson 1983). Based on size meas- fied habitat patches and microhabitats that we urements of animals, we produced a regression could easily categorize. Each survey was equation relating measured total lenght (M) to designed to represent only one of four habitat estimated total length (E). categories: lake, river, river-lake, and stream. The length of the survey routes were These categories are self-explaining, except determined in two ways: (a) by standing the river-lake, that refers solely to long islands, limits from geographical references esta- with great lakes inside and separated by wide blished during fieldwork, or (b) by ploting pre- channels (Figs. 1, 2). For every individual cise geographical coordinates obtained with caiman encountered, we assigned one of nine the Global Positioning System Receiver microhabitat classifications (considering vege- Garmin¨ 45. The distances traveled were tation type, water depth and flow) designated measured on a drawn map of JNP (produced as: (1) Grass: constitutes the floating grass by Fundação Vitória Amazônica-FVA, based carpet; (2) Rapids: include shallow waters with on Landsat-TM images), with flexible ruler (in swift running current; (3) Pool: deep waters 1098 REVISTA DE BIOLOGêA TROPICAL

Fig. 1. Surveys and habitats in the Central study area of Jaú National Park. River habitats (3, 9, 13), Stream habitats (2, 8, 14). Survey number legend as Table 2. Clipping of Landsat TM image 1 : 250 000. Detail: location of JNP in Brazil.

Fig. 2. Surveys and habitats in the Rio Negro study area of Jaú National Park. River-Lake habitats (18, 19, 22), River habitats (1, 5, 16, 17), Stream habitat (4), Lake habitat (6). Survey number legend as Table 2. Clipping of Landsat TM image 1 : 250 000. INTERNATIONAL JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 1099 with no current; (4) Deep: the deep waters with or surveys into groups or clusters. These clus- swift moving currents; (5) Stream Igapó: ters may delimit or represent different croco- flooded forest with little current, short flooding dilian assemblages based on their overall period, and high plant diversity; (6) Land: all resemblance. A possible random utilization of land locations including animals on sandbank, resources can be indicated by no structure. But mud beaches, rocks, and clay banks; (7) if there are any ecological separations and Margins: shallow waters with little or no cur- associations between species, well-defined rent; (8) Lake Igapó: flooded forest with no clusters of surveys can emerge using hierarchi- current, longest flooding period, and lowest cal, agglomerative and polythetic classifica- plants richness; (9) River Igapó: flooded forest tions with species abundance data, which can with little current, but intermediate flooding be summarized in a dendrogram (Ludwig and period and plant richness. Reynolds 1988). The data of abundances For search of species associations, we matrix were added to a constant (0.01), log- constructed a presence-absence matrix with transformed and relativized by standard devi- surveys as columns and caiman species as ates of species abundances. The distance meas- rows, and then calculated Jaccard Distance ure used was relative euclidian and the group (JD) as follows: linkage method was median. Cluster analyses 1-2W/(A+B-W) were performed using Pc-ord 2.01 software (McCune and Mefford 1995). Voucher speci- where W is the sum of shared abundances and mens were deposited in the herpetology collec- A and B are the sums of abundances in indi- tion of the Instituto Nacional de Pesquisa da vidual sample units. Amazônia in Manaus, Brazil. We used another matrix of quantitative measures of species abundance (surveys as columns and species as rows) to identify RESULTS species correlations (covariation of abundances between species) (Ludwig and Reynolds 1988). We used Spearman correla- Distribution and abundance: During the tion coefficients to determine species affini- sampling, we identified 290 individuals. ties. All indexes, calculations and statistical Species observed were common caiman (C. tests, were performed using Systat 5.03 crocodilus), black caiman (M. niger), (Anonymous 1990-1993). Schneider’s caiman (P. trigonatus), and dwarf We used Cluster analysis to examine croc- caiman (P. palpebrosus). Common caiman odilian assemblage structure (an uncommon was the most frequently observed (69 %), fol- procedure, since crocodilian studies usually lowed by black caiman (14 %), Schneider’s were focused on one species), because this caiman (12 %), and dwarf caiman (4 %) across classification technique places similar samples all surveys combined (Table 1).

TABLE 1 Number of crocodilians sighted within species and size classes in Jaú National Park during 1993-1996 nocturnal spotlight surveys

Numbers in size classes* Species N H 2 - 6 6 - 10 10 - 14 14 - 18 18 - 22 > 22 NR Caiman crocodilus 201 44 25 53 38 28 7 1 5 Melanosuchus niger 40 8 4 5 3 6 11 3 Paleosuchus trigonatus 36 14 11 8 3 Paleosuchus palpebrosus 13 2 3 8

* Size classes in m x 10-1. N: total crocodilians sighted. H: hatchlings. NR: size not estimated. 1100 REVISTA DE BIOLOGêA TROPICAL

The abundances of species varied across Distrance (Objetive Function) surveys (Table 2). We surveyed 371 km of 1,4E-01 2,7E-01 4E-01 5,4E-01 6,7E- shoreline, 287 km during the wet season (20 Information Remaining (%) surveys) versus 84 km in the dry season (10 100 75 50 25 0 surveys). The total number of caimans (i.e., all CC species combined) observed in the dry season surveys (1.1 + 0.5 caimans/km) was greater MN than in the wet season (0.9 + 0.5 caimans/km), but these differences were not significant PP between seasons (t0.05(2),28 = 0.829, p > 0.5). The higher abundance (2.3 caimans/km, two species, stream habitat) was observed in wet PT season. The second highest abundance Fig. 3. Crocodilian species associations in Jaú National (2.2 caimans/km, one species, lake habitat) was Park, from a presence/absence matrix based on data of observed in dry season. Table 2. Measure distance was Jaccard coefficients and Therefore the mean caiman abundance group linkage method was Centroid. CC: Caiman croco- was 1.0 + 0.5 caimans/km. Low abundance dilus, MN: Melanosuchus niger, PP: Paleosuchus palpe- surveys predominated: in 17 surveys we count- brosus, PT: P. trigonatus. ed less than 1.0 caiman/km, while in eight surveys we observed moderate abundances palpebrosus (0.333), and revealed that there is (1.0-2.0 caiman/km). The highest abundances no association (or complete exclusion) between were observed in less disturbed areas, while M. niger and P. trigonatus. the lowest abundances were observed in more Similarity among surveys may be disturbed areas. The ranges of abundances were expressed by measuring the correlation similar between rivers (0.3-2.1 caimans/km), between species abundances. There was a lakes (0.6-2.2 caimans/km) and streams small negative correlation between C. croco- (0.5-2.3 caimans/km), but was minor in river- dilus and P. trigonatus that was significant lake surveys (0.2-1.2 caimans/km). (-0.459, ANOVA1,27 F = 5.501, p = 0.027) and No caiman species were distributed con- a positive, but not significant (0.401, p = 0.08) tinuously across the entire study area. The correlation between P. palpebrosus and P. trig- common caiman ocurred in 25 surveys (mean onatus. There was a small covariation of C. abundance 0.4 + 0.3 caimans/km), the black crocodilus and M. niger abundances that was caiman was observed in 12 surveys highly non-significant (0.004, p = 0.900). The (0.2 + 0.1 caimans/km), Schneider’s P. trigona- structure of caiman assemblage does not tus was observed only in five surveys (but with ressemble a pattern of separated sets of species mean abundance of 0.6 + 0.3 caimans/km), and associated to specific habitats. The only actu- P. palpebrosus was observed in seven surveys al trend we observed in species relationships (mean of 0.1 + 0.1 caimans/km). was that populations of similar size species (C. Comparing the species composition crocodilus and P. trigonatus) were mutually between surveys we found two groups: C. croc- excludents and may have a niche overlap. odilus - M. niger, and P. trigonatus - P. palpe- Size-age structures: In order to correct brosus (Fig. 3). Despite the coefficient of com- estimated total length of observed, and not munity does not take into account the relative captured animals, a linear regression line abundance of species assemblage, we measured of predicitive size was used for all species the differences in community structure and (M = 0.004 + 0.966 E, F1,18 = 60.046, expressed the relative weakness of the two pos- p < 0.001, R2 = 0.757) (Fig. 4). Frequency dis- sible associations, the pair C. crocodilus - M. tributions of estimated size for black caiman niger (0.480) and the pair P. trigonatus - P. and dwarf caiman were skewed toward the INTERNATIONAL JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 1101 . Study areas: RN: Rio Negro, hatchlings. Paleosuchus trigonatus , PT: , PT: M. niger Paleosuchus palpebrosus ABLE 2 , PP: T ype Area CC MN PP PT Eyes Total Pods count T Surveys of caimans in Jaú National Park. Melanosuchus niger , MN: Caiman crocodilus iratucu Jul,19,93 03:23 Stream CE 21.6 W 0.00 0.00 0.00 0.78 0.21 0.99 Preto Oct,19,93 02:20 Stream RN 4.9 D 0.82 0.00 0.20 0.20 0.41 1.63 Surveys Dates H (hours) Habitat Study km Season Caimans/km Hatchlings Jaú mouth Jul,17,93 04:00 River RN 11.7 W 0.43 0.08 0.00 0.00 0.17 0.68 Supiá Lake Oct,20,93 00:32 Lake RN 4.9 D 2.04 0.00 0.00 0.00 0.20 2.24 Umanapana Jan,24,94 02:10 Stream CE 6.4 W 0.00 0.00 0.31 0.62 1.41 2.34 Cutiuaú Lake Oct,29,93 04:02 Lake CT 11.5 D 0.96 0.26 0.00 0.00 0.09 1.31 Miratucu (lower) Jan,17,94 02:12 Stream CE 9.0 W 0.00 0.00 0.00 0.89 0.22 1.11 C.Grande-Miratucu Jul,29,93 02:15 River CE 11.0 W 0.45 0.00 0.00 0.00 0.54 0.99 Miratucu mouth-Catoá Jan,17,94 03:32 River CE 7.7 W 0.78 0.13 0.13 0.00 1.04 2.08 1 8 Preto mouth-Manichuau Oct,20,93 01:11 River RN 8.3 D 0.36 0.00 0.00 0.00 0.36 0.72 8 9 7 1 2M 4 5 6 3 11 12131415 Macaco mouth-Maranhoto16 Jan,30,94 Miratucu mouth-Pajé17 03:0118 Miratucu (Gerley) River19 Feb,15,94 02:5320 Moura-Nazaré CE Uruá-Jaú mouth21 Feb,18,94 River 03:0022 Negro (Enseada) 21.6 Stream23 CE Mar,05,94 Negro Negro (Panema) Sep,02,94 03:0524 01:00 CE Negro (Onças)25 W Lake 20.1 Apr,07,95 River26 02:36 Jaú mouth Apr,08,95 River/Lake 0.37 Negro (Grande)27 14.0 S.Maria-Praia Alta 05:34 CT W RN RN River/Lake Apr,06,9528 Apr,09,95 0.00 03:12 RN S.Maria-Feijão 04:2229 W 0.20 River/Lake 12.4 Sep,01,95 18.530 River Jan,19,96 0.00 4.0 RN 04:01 Apr,10,95 0.00 02:37 River/Lake 0.00 24.5 Cutiuaú Lake 03:00 Unini (Sumaúma) Pinto 0.00 W RN RN W River Jan,23,96 0.00 32.3 River 0.05 D 02:33 0.28 W 0.89 0.05 Papagaio Unini (Tapiira) WE 0.14 0.00 Sep,05,96 14.3 21.6 River 0.25 RN 0.65 Jan,25,96 W 0.53 01:43 0.00 01:18 0.16 0.05 0.36 Mauaru 0.75 12.3 WE Jan,21,96 W Lake 0.22 D 0.00 14.3 0.00 Lake Sep,14,96 0.50 0.00 01:50 0.30 0.00 01:54 0.35 Sep,11,96 0.03 River/Lake 0.00 0.37 W 0.00 River 5.9 0.00 U 1.00 01:06 CT W 0.00 U 0.00 0.00 0.00 0.32 0.16 0.00 0.00 River WE Sep,17,96 0.21 0.25 W 02:10 0.28 0.00 1.2 0.00 1.21 6.5 0.00 0.21 0.00 7.7 Stream U 1.25 0.07 13.6 0.17 0.28 0.81 0.00 0.00 2 0.08 D W 0.00 U 0.14 0.34 0.53 2 0.37 W D 12.0 16 0.00 0.15 0.00 0.00 0.49 0.17 0.74 0.22 0.16 8 0.65 7.7 0.56 D 0.00 0.00 0.00 0.40 0.22 0.00 0.84 0.08 0.00 0.00 0.51 D 0.00 0.00 0.00 1 0.00 0.16 1.19 0.13 0.00 0.00 0.46 0.81 3 0.00 0.29 0.52 0.13 0.61 0.81 0.00 0.73 1.17 0.00 0.25 2* 0.00 0.50 9 0.26 1 0.52 4 10 Macaco Jan,23,94 01:12 Stream CE 9.3 W 0.54 0.32 0.00 0.00 0.32 1.19 CE: Central, CT: Cutiaú, WE: West, U: Unini. Seasons: W: wet season, D: dry season. * including one pod of W: U: Unini. Seasons: West, WE: Cutiaú, CE: Central, CT: H: duration of observation period, CC: 1102 REVISTA DE BIOLOGêA TROPICAL

2.0 (3) river-lakes (inhabited by the C. crocodilus - M. niger pair). Moderately similar were (4) rivers and river-lakes, (5) rivers and lakes, and (6) rivers (inhabited by C. crocodilus - 1.5 M. niger pair, with occasional P. palpebrosus). Dissimilarities were higher among (7) streams, (8) rivers and streams, (9) streams and river- lakes, and (10) streams and lakes. 1.0 Surveys in streams were not quite homo- geneous, they were different within stream surveys and different in each stream, among

Measured total length (cm) Measured upper and lower courses of the stream. In some stream surveys, we found P. trigonatus 0.5 0.0 1.5 1.0 1.5 2.0 populations, but in others we did not. Estimated total length (cm) The examination of microhabitats used by caimans (Fig. 5) suggests a thin habitat parti- Fig. 4. Relationship between estimated and measured size of a sample of caimans captured at Jaú National Park. tioning. Paleosuchus trigonatus were absent Regression line: Measured = 0.004 + (0.966) Estimated. from river and lake Igapó, but were frequent in 2 F1,18 = 60.046, R = 0.757. stream Igapó. This species was the most terrestrial and frequently observed on land. The only microhabitat category that they used as larger size classes, which were expected for frequent as C. crocodilus were margins. long-lived species with continual growth. However, P. trigonatus was frequently Large M. niger include some 4 m long individ- observed in water as deep as M. niger. uals, while large P. palpebrosus has animals of The most frequently used microhabitat by 1.0-1.4 m in length. The length frequencies for C. crocodilus and M. niger were river and lake C. crocodilus showed a predominance of juve- Igapó, but this two species differ in use of niles and subadults, and for P. trigonatus a pre- other microhabitats: C. crocodilus predomi- dominance of middle size classes of subadults. nate in shallow waters (margins) and land loca- Few juveniles were observed. Among tions, while M. niger predominated in deep common caiman, eight pods of hatchlings were moving waters, but were absent from stream observed, 22 % of individuals of these species Igapó. Carpets of floating grass are rare in were juveniles, most observed in the early wet JNP and only C. crocodilus was observed in season (six pods in Rio Jaú and one pod in Rio such habitat. Negro), and one in early dry season (Rio Paleosuchus palpebrosus was observed Unini). Common caiman pods were observed only in running water microhabitats: river in nearly every habitat type, but mostly in river Igapó, margins, stream Igapó and rapids, and habitats. Juveniles composed 20 % of the never in stagnant waters of lake habitats. Only overall observations of black caiman, that cor- Paleosuchus was observed in fast running responds to one pod of hatchlings observed in rapids. upper Jaú in the early wet season. No juvenile The general pattern of microhabitat use Schnider’s or dwarf caimans were observed. was strongly oriented to river Igapó, lake Species-habitat relations: Comparing the Igapó and margins (30 %, 20 %, and 18 % of species composition between surveys using observations, respectively). coefficients of community (Jaccard) for habitat Assemblage structure: The patterns of categories, we found differences. Ranking the clustering of surveys were summarized in the mean coefficients for habitat, the most similar dendrogram in Fig. 6. Using an arbitrary cut- were (1) lakes, (2) lakes and river-lakes, and off distance of 4.3, we distinguish three clus- INTERNATIONAL JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 1103

Fig. 5. Microhabitat used by caimans in Jaú National Park. CC = Caiman crocodilus, MN = Melanosuchus niger, PP = Paleosuchus palpebrosus, PT = Paleosuchus trigonatus, I. = Igapó.

ters, which can be described only by species composition: Cluster A represents surveys where we find C. crocodilus and M. niger. Cluster B represents surveys where we find only C. crocodilus populations. Both patterns were common and observed in all habitats types and study areas, making a mosaic. Cluster C represents some of the most rich in species surveys, but what was distinctive was the presence of at least one Paleosuchus in all these surveys, in river and stream habitat types, in Central and West study areas. Populations of P. trigonatus were find only in streams, and P. palpebrosus in river and streams. Human impact: Long term human disturbance of this ecosystem was not much evident. We observed a mild slight trend to increase wariness, that could be attributed to human general activities in JNP. The proportion of eyes observed in much disturbed localities (40 %) was greater than in little disturbed ones (38 %), but this diference was not significant Fig. 6. Cluster analysis of surveys of caimans of Jaú (t = 0.269, p > 0.5). We observed, National Park, based on the abundance data of Table 2. 0.05(2),28 Data added to a constant (0.01), log-transformed and rela- however, an increase of wariness that could be tivized by standard deviates of species abundances. attributed to our surveys. When we compared Distance measure was relative euclidian and group linkage the proportion of eyes in consecutive surveys, method was Median. Percent chaining: 7.53. Clusters: A: there was a trend to increase the proportion of surveys with Melanosuchus niger and Caiman crocodilus wariness with time in all habitats and study set, B: surveys with only Caiman crocodilus, C: surveys with at least one Paleosuchus species. Survey number areas, considered by us disturbed or not. Three legend as Table 2. sequences of three surveys (surveys # 1, 16, 1104 REVISTA DE BIOLOGêA TROPICAL and 21 in Jaú mouth, surveys # 2, 8, and 14 in To compare this study with published surveys Miratucu stream, and surveys # 7, 15, and 26 carried out in Amazonian waters, Glastra in Cutiaú lake) and one sequence of five sur- (1983), Espinosa (1995), Brazaitis et al. veys (# 17, 18, 19, 20, and 22 in Rio Negro), (1996a), Da Silveira et al. (1997) and Da all showed clearly similar increasing wariness Silveira and Thorbjarnarson (1999) reported trends. values between 1-19, 0-2, 0-10, 0-58 and 1-115 caimans/km, respectively. The abundance obtained in this study (0-2 caimans/km) DISCUSSION was low in comparison with the majority of values from other caiman surveys in This study focused on distribution and Amazonian waters. But, abundances reported abundance of the caiman community of Jaú by Da Silveira and Thorbjarnarson (1999) of National Park as they related to habitat carac- very abundant populations of C. crocodilus teristics. The presence and relatively stable and M. niger in Mamirauá reserve sector’s abundance of common species at each study where hunting pressure is lowest, is a rare site show that these species had wide distribu- event in Amazonia. tions along the area. However, the abundance The distribution of common caimans of each species varied in association with dif- reflects their general habitat use as was seen in ferent habitats and as a response to species other studies (Medem 1971, 1981, 1983, interactions. The small relative abundances Magnusson 1985, Brazaitis et al. 1990, 1996a, b). could reflect bias due to wet season dispersal, Surveys where we observed only one species since in JNP environmental disturbance are always had C. crocodilus in floodplain, or P. minimal, and there is no marginal habitats. trigonatus in streams of the Central study area. Differences between dry and wet seasons sur- Melanosuchus niger and P. trigonatus were not veys could indicate the existence of many indi- observed together in any survey, maybe viduals unapparent in the wet season. because of mutual exclusion, although the lit- Caiman surveys in South American savan- erature recorded sympatric occurrence of the nas observed large differences of abundance two species (Medem 1967). between seasons, and the dry seasons abun- In previous studies M. niger populations dances could be two to ten times larger than were so reduced, that it was impossible to deter- the wet season abundances (e.g. Gorzula 1978, mine which is the relationship between that Glastra 1983). But the similar numbers species and C. crocodilus (Brazaitis et al. 1996a, between dry and wet seasons in JNP, suggests Da Silveira et al. 1997). The authors explained that there should not be a great number of the small numbers as evidence of very reduced caimans hidden inside the flooded forest. populations due to commercial hunting: few M. Juveniles of C. yacare have been reported to niger survivors were observed “mixed” with sev- occur somewhat appart from adults and in eral C. crocodilus, which could be contributing shallower waters (e.g. Rebêlo et al. 1997). (as predators or competitors) to hinder the recov- However, we assumed that because the same ery of the populations of M. niger submitted to survey method and similar effort were used hunting (Magnusson and Rebêlo 1982, Rebêlo among surveys, observational bias remained and Magnusson 1983). However, without strong consistent and the observed differences in evidences of species interference, differences in abundances for each species likely reflects the distribution of sympatric populations were attrib- caiman assemblage structure in JNP. uted to habitat preferences (Magnusson 1985). The very low densities of fewer than Therefore, reduced populations of M. niger were 1 caiman/km that we detected were reported in considered unable to affect the distribution of C. 70 % of the localities surveyed elsewhere in crocodilus (Da Silveira et al. 1997), while the Amazonian waters by Brazaitis et al. (1996a). reversal is unknown. INTERNATIONAL JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 1105

The different adult size of the two species to deal with water speed: in his analysis and the differential use of microhabitats, could Paleosuchus are caimans of (1) running waters reduce or attenuate the negative effects of shar- of tropical forest streams with rocky or sandy ing the same habitats and eating similar preys. bottom, (2) neighbourhood of rapids, water- In the blackwater Archipelago of Anavilhanas, falls, jumps and whirls, (3) narrow channels of C. crocodilus abundance does not coincide large rivers through where masses of water with food availability and nesting areas of M. slide swiftly (as in narrow pass), and (4) savan- niger, which predominate in the deeper water na streams and gallery forests. channels, with more sediments and floating For Medem (1967, 1971), P. trigonatus grass (Da Silveira et al. 1997). would represent the primitive form, while The non occurrence of the four species in P. palpebrosus would be the most specialized. all surveys suggests effective habitat partition- Paleosuchus palpebrosus would have devel- ing. Melanosuchus niger and C. crocodilus oped adaptations to colonize the larger bodies inhabit floodplain habitats, while P. trigonatus of water, where there is some water flow (as a inhabits forest streams and turbulent waters secon-dary effect, the “carapace” guaranteed (Medem 1981, 1983), and their peculiar diet an extra protection against drying up in unfa- was attributed to habitats selection (Magnusson vorable habitats and against predation from et al. 1987). Notwithstanding, our results of larger species). streams with C. crocodilus and M. niger chal- If the flow is the critical factor, the resis- lenge strictly the habitat separation hypothesis, tance to impact on rocks and the swimming despite the absence of P. trigonatus in river and capacity would be factors capable to increase lake habitats. The importance of interspecific or to reduce the fitness of a species. competition in the organization of crocodilian Magnusson (1989) commented that “It is obvi- communities is easy to imagine since they are ous that the habitats of each [Paleosuchus] dif- members of the same guild, but is difficult to fer, and that the habitats of both are different establish since the mere presence of differences from those of other sympatric crocodilians but of resource utilization between species is not just which differences are critical remains con- evidence of competition (Schoener 1974), and if jecture.” According to Magnusson (1989), P. other factors (as predation, food, weather, or trigonatus is the specialized form differing something else) keep densities at a low level, from the other crocodilians in its thermal bio- the role of competition will be negligible logy (living in moderate temperature and rela- (Begon et al. 1996). tively stable forest habitat, with limited oppor- Physiological and behavioral mechanisms tunities for basking), and may be the largest can also reduce or attenuate the niche overlap biomass of great predators in the Terra Firme between species. Nests of P. trigonatus need an forest near Manaus, drained by small streams extra source of heat (Magnusson et al. 1985) (Magnusson and Lima 1991). while the C. crocodilus females build common In JNP, P. trigonatus is not the only mound nests (Gorzula and Seijas 1989). Adults species of forest streams, and different from of C. crocodilus prey upon fishes and large the Manaus area, most of the individuals we invertebrates, while adults of P. trigonatus prey observed were subadults, a stage of life with mostly on terrestrial vertebrates (Magnusson et high dispersion rates (great mobility). In the al. 1987). Paleosuchus trigonatus have a high- Manaus semi-urban area, most of the popula- ly terrestrial life (Magnusson and Lima 1991) tion was constituted by adult animals, whose while C. crocodilus spend most of the day in the high survival rate and extended lifetime would water (Marcellini 1979). have great influence on the population dynam- We observed P. trigonatus in 71 % of the ics (Magnusson and Lima 1991). stream surveys. Medem (1967, 1971) remar- Conservation: We used a regression line ked that what separate the species is any skill to correct size estimates, a usually neglected 1106 REVISTA DE BIOLOGêA TROPICAL tool. The action plan for crocodilian conserva- (Da Silveira and Thorbjarnarson 1999) and tion of the Crocodile Specialist Group current evidences of localized recovery are (Thorbjarnarson 1992), call for more popula- supporting a proposal to downlist M. niger in tion survey work, that was “urgently needed Brazil (Ronis da Silveira pers. comm.). As for a large percentage of the [crocodilian] large caiman populations are rarely found, we species”. Surveys were considered needed not do not support the increase of utilization of M. only for planning recovery programs, but also niger and the efforts to widespread use of the as the first step of sustainable yield utilization species. projects. However, rarely the relationship The discovery of small populations of M. between actual and estimated sizes of indivi- niger in scattered distributions throughout duals has been presented, and accurate esti- Amazonia, are considered an effect of overex- mates of total numbers are of limited use with- ploitation (Plotkin et al. 1983, Brazaitis et al. out some idea of the accuracy of the size esti- 1996a, b, 1998), and does not fit the historical mates (Magnusson 1983). records that reported larger populations (Bates These data provide the first comprehen- 1876, Carvalho 1951, Aguirre 1956). Small, sive overview of the caiman community in disjunct, isolated populations that are reported JNP. For common and black caimans in this do not mean that the species has recovered areas, populations are currently widespread in everywhere and can not support the efforts to floodplain, but appear to be not abundant. reassessment of the status of the species and Schnider’s caiman is specific of some streams. allow it in the trade. The rare but widespread observation of dwarf We do not know what was the level of dis- caiman suggest that the species is a habitat turbance that the caimans of JNP experienced generalist, but its abundance may be affected in the past. If measures of wariness reflect such by the other species. Their use of the river, disturbance (and we agree that it may reflect however illustrates the importance of riverine very recent episodes), our study shows that systems to all caiman species found within researchers disturbed the caimans more than JNP. local inhabitants. Based on reports of local The differences in numbers of different inhabitants, we can say that where today is the species show the influence of different habitat JNP, commercial hunting of C. crocodilus and caracteristics and patterns on caiman assem- M. niger stopped in 1973. This could be con- blages. The river and lake Igapó were impor- sequence of legal prohibition or depletion of tant to common and black caimans, the deep population stocks. waters attracted more black caimans, and the Current inhabitants cause little impact on stream Igapó and rapids were preferred by caiman populations, but this is not because Paleosuchus. there is hunting restriction, since it is also for- Very low numbers of caimans were bidden the commercial fishing of turtles. They present in JNP , but the observation of pods of catch turtles once there is market for them. hatchlings suggests that there is successful Now, local inhabitants rarely eat caiman meat, reproduction of the two most abundant species. or kill large and potentially dangerous animals. Without immediate threats of habitat destruc- However, when the fashion comes back, we tion, with large areas of pristine habitats, the must be aware about the management and con- situation has been favorable for the recovery of servation of the low density populations in the populations affected by commercial hunt- poor blackwater areas. ing in the past. The international trade in The aquatic ecosystems of the Amazonia caiman skins periodically increase the demand blackwater rivers and streams constitute nutri- for all crocodilian-skin products, touted by the ent poor areas, considered uncapable to main- fashion industry (Brazaitis et al. 1998). The tain populations as large as the ones reported regional market for caiman meat is increasing for “white waters” (loam silted rivers). INTERNATIONAL JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 1107

Blackwater rivers are considered acid, low de Aperfeiçoamento de Pessoal de Nível nutrient, high nitrogen ecosystems with head- Superior (Bolsa de Doutorado para GHR); and waters inside forests with sandy podzols soils Instituto Brasileiro do Meio Ambiente e dos (Sioli and Klinge 1962). Blackwater rivers and Recursos Naturais Renováveis. This paper is the lands they drain have low subsistence part of GHR doctorate thesis in Ecology at potential for human populations and they are Universidade Estadual de Campinas. notorious “starvation rivers” (Meggers 1996). As top predators even the caiman populations should be limited by habitat productivity. REFERENCES Small populations have a general problem in conservation biology, since they can be at risk Aguirre, A. 1956. Contribuição para o estudo da biologia simply because of their size, which requires do jacaré-açú Melanosuchus niger (Spix). Ministério da Agricultura - Divisão de Caça e Pesca, Rio de studies on the effects of low numbers on pop- Janeiro. 15 p. ulation persistence (Caughley and Gunn 1996). Thus the factors that are limiting these popula- Anonymous. 1990-1993. Systat 5.03 for windows. tions, however, can be independent of human Evanston, Illinois. exploitation. Anonymous. 1998. Plano de manejo do Parque Nacional do Currently, in Amazonia increased the Jaú. Fundação Vitória Amazônica, Manaus. 258 p. pressure of hunting, habitat loss and habitat alteration, and there is no evidence of wide- Bates, H.W. 1876. The naturalist on the river Amazons. spread recovery of caiman populations. Our John Murray, London. 300 p. (Tradução Regina R. data show that in large reserves without many Junqueira) disturbances, most caiman populations can Bayliss, P. 1987. Survey methods and monitoring within have low density, suggesting that in blackwater crocodile management programmes, p. 157-75. In G. environments their recovery from exploitation Webb, C. Manolis & P. Whitehead (eds.). Wildlife should be very slow. management: Crocodiles and Alligators. Surrey Beatty, Chipping Norton, Australia.

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