Caribbean Journal of Science, Vol. 42, No. 3, 380-385, 2006 Copyright 2006 College of Arts and Sciences University of Puerto Rico, Mayagu¨ez
Differences Between Epigeic Earthworm Populations in Tank Bromeliads from Puerto Rico and Dominica B. A. RICHARDSON1,*, S. BORGES2 AND M. J. RICHARDSON3 1,3
Associate Scientists, Luquillo LTER, Puerto Rico, and 165 Braid Road, Edinburgh EH10 6JE U.K. 2 Department of Biology, University of Puerto Rico, Mayagüez, Puerto Rico 00681 3 *Corresponding author:
[email protected]
ABSTRACT.—Large differences were found between the abundance, biomass and distribution of epigeic earthworms in the bromeliads of montane forests in Puerto Rico and Dominica. In Dominica they occurred in more than 90% of plants and made up 60-80% of the total invertebrate community biomass, whereas in Puerto Rico they were only found in 8% of plants and were less than 2% of invertebrate biomass. In Dominica, therefore, these worms are likely to have a major role in processing canopy litter falling into bromeliad rosettes, as other groups of leaf processors, such as Isopoda and Diplopoda, were relatively infrequent. Conversely, in Puerto Rican bromeliads, where earthworm abundance was low, Isopoda and Diplopoda comprised a higher proportion of the invertebrate community. The earthworm species occurring in the two islands were different, Neotrigaster complutensis and Trigaster yukiyui in Puerto Rico, and Eutrigaster sporadonephra in Dominica. The biogeography of epigeic worms in bromeliads is briefly discussed. KEYWORDS.—biomass, Eutrigaster, Megascolecidae, Neotrigaster, phytotelmata, Trigaster.
INTRODUCTION Tank bromeliads are important components of the epiphytic vascular flora of neotropical forests, increasing in density at higher elevations (Richardson 1999). Their rosettes are adapted for capture and retention of water and canopy debris. Benzing (1986) categorized these plants as ‘animal assisted saprophytes’, since litter intercepted from the canopy is consumed and reduced to finer particles by their considerable detritivore communities. Nutrients from decomposition and animal waste are absorbed by the plants via specialized trichomes at the bases of the leaves that form water-filled tanks (phytotelmata). Many organisms are bromeliad specialists, but there is no evidence of species-specific associations between particular bromeliad species and their faunas (Benzing 1990). In Puerto Rico, breakdown of new litter in bromeliad rosettes is initially brought about by microbial activity and shredders
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such as millipedes, isopods and cockroaches, which are also found in forest floor litter. Fine particulate organic matter is washed into the tank and further consumed by a variety of semi-aquatic and aquatic larvae (largely Diptera and Coleoptera) and adult beetles living in the spaces between the closely appressed leaves and in the phytotelm (Richardson 1999; Richardson et al. 2000; Richardson et al. 2005). Epigeic earthworms, which do not inhabit fixed burrows, but normally live in litter, under bark of rotting trees, etc., have been observed in tank bromeliads by Laessle (1961) in Jamaica, Picado (1913) in Costa Rica, and other authors, but little has been reported on either their identity or abundance. Fragoso and Rojas-Fernández (1996), however, reported the presence of Eutrigaster sporadonephra (Cognetti, 1905) (Oligochaeta, Megascolecidae) inhabiting decaying logs and bromeliads in a Mexican seasonal tropical rain forest, and quantified its occurrence and abundance. It was found almost exclusively in bromeliads. Two other megascolecid species were also found in these Mexican bromeliads, but in very
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low numbers. Nine species of Dichogaster were described by James (1996), from the island of Guadeloupe, six of which were found to inhabit bromeliads. In Dominica we found E. sporadonephra, large blue worms, to be the main component of the tank bromeliad community. We report the details of their abundance, frequency and biomass compared with occurrence of the few epigeic oligochaetes found in the bromeliads of Puerto Rico and populations reported by Fragoso and Rojas-Fernández (1996) from Chajul in Mexico. MATERIALS AND METHODS The invertebrate communities of whole bromeliad rosettes (Guzmania and Vriesea spp.) were obtained by collecting plants and their retained water and debris in the field. In the laboratory, plants were dismantled leaf by leaf. The leaves were washed in water, and all leaf washings retained for examination, together with the original tank water. All organisms were collected into alcohol, identified to morphospecies, and measured so that estimates of biomass could be obtained. Biomass was calculated using length/dry weight relationships obtained during the course of this and other studies (Richardson et al. 2000, 2005), and archived at http://luq.lternet .edu/data. Study area Puerto Rico.—Bromeliads were collected in the Luquillo Experimental Forest (LEF, NE Puerto Rico, 18°N, 65°W) from three main areas, tabonuco forest at El Verde (ca 350-450 m.a.s.l., 70 plants), palo colorado forest from the Trade Winds and El Toro
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Trails (750-900 m.a.s.l., 60 plants), and dwarf forest at Pico del Este (900-1050 m.a.s.l., 60 plants). Collections were made over 4 periods from December to March 1993/4, 1994/5, 1996, 1997. Additional collections of ten plants each were made at 13 points on an elevational transect on the Quebrada Sonadora in the LEF, at vertical intervals of 50 m from 400-1000 m.a.s.l., in January/February 2003 and 2004, and from El Yunque (LEF) and Toro Negro in the Central Mountains (955-1330 m.a.s.l) in January/February 2005. Rainfall varies from ca 3.5 m/year in the tabonuco forest to ca 5 m/year in the dwarf forest (GarcíaMartinó et al. 1996). A total of 340 plants was sampled. Dominica.—Collections of bromeliads were made in February 2002, 10 plants each from tabonuco forest on Morne Trois Pitons (15.4°N, 61.3°W, 775-850 m.a.s.l.), in midelevational montane thicket at Boeri Lake (15.4°N, 61.3°W, 800-850 m.a.s.l.), and from cloud (elfin) forest on Morne Diablotins (15.5°N, 61.4°W, 1100-1160 m.a.s.l.). Rainfall in all three forests is ca 6-7.5 m/year (Evans and James 1997). RESULTS In Dominica, Eutrigaster sporadonephra was common at each of the three sites sampled; occurring in 90-100% of plants (Table 1). Their pattern of occurrence was aggregated, with two-thirds of the plants having five or more worms (Fig. 1), and both adult and juvenile individuals were present. The number of individuals increased with the size of the bromeliads (Fig. 2). The highest count was 25 which, incidentally, was the same as the highest
TABLE 1. Abundance and frequency of epigeic earthworms in bromeliads from Puerto Rico (Neotrigaster Yukiyui and Trigaster complutensis) and Dominica (Eutrigaster sporadonephra), and other major litter processors Puerto Rico
Tabonuco Mid-elevation Cloud forest
Dominica
Earthworms
Isopods
Diplopoda
Earthworms
Isopoda
Diplopoda
*0.12 (5) 0.09 (8) 0.04 (4)
10.8 (54) 15.0 (89) 2.4 (60)
0.6 (31) 1.7 (64) 0.5 (23)
5.5 (90) 12.6 (90) 9.8 (100)
0.7 (40) 1.4 (60) 0.6 (30)
0.2 (20) 0.1 (10) 0.2 (20)
*Mean no./bromeliad and, in parentheses, % of bromeliads occupied.
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FIG. 1. Pattern of occurrence and abundance of epigeic earthworms in Dominican, Puerto Rican and Mexican bromeliads (Mexican data from Fragoso and Rojas-Fernández (1996)). Data expressed as % values for comparison.
number found by Fragoso and RojasFernández (1996) in Mexican bromeliads. Eutrigaster sporadonephra was not found in Puerto Rico. Instead, the earthworms Neotrigaster complutensis (Borges and Moreno 1991) and Trigaster yukiyui Borges and Moreno 1991 were occasionally collected, occurring in less than 6% of plants overall (Table 1), with a maximum of seven being found in any one plant, and 13 of the 28 worms being a single individual (Fig. 1). Descriptions of these latter two species are given in Borges (1996). As a consequence of their size and abundance, E. sporadonephra comprised a major part of the total invertebrate biomass in Dominican bromeliads (Table 2), at a maximum in cloud forest at 81% and present in all plants sampled. The main litter processors in the Puerto Rican bromeliads, in all forests, the isopods and millipedes, were relatively infrequent and comprised only a very small component of the Dominican bromeliad invertebrate biomass (Table 2). Conversely, in Puerto Rico, the epigeic worms (N. complutensis and T. yukiyui) comprised only 2% biomass at a maximum in the tabonuco forest, with isopods and millipedes having a much higher abundance and biomass (Table 2). The differences in comparative abundance of earthworms, isopods and millipedes in bromeliads between Dominica and Puerto Rico (Table 1) are highly significant, P < 0.0001 (earthworms vs diplopods, 2 = 372,
FIG. 2. Relationship between number of Eutrigaster sporadonephra worms in Dominican bromeliads and plant size. Regression equation: y = 0.287x. −6.17, R = 0.58 (P < 0.005).
2 d.f. and earthworms vs isopods, 2 = 1810, 2 d.f.). DISCUSSION These three earthworm genera are all native to the north Neotropics (Fragoso et al. 1995). None are common, and seem to be restricted to more or less remote habitats distant from human influence (Gates 1962). Little is known of their habits and distributions. Fragoso and Rojas-Fernández (1996) mention that the aboveground habitat colonization by earthworms may be a temporary situation or a permanent response to ecological factors, such as soil water saturation or acidity. The low frequency of worms in Puerto Rican bromeliads suggests that N. complutensis and T. yukiyui are only occasional visitors of these plants. Neither of these species seems to be a bromeliad specialist and, until now, they have always been collected from the ground. Some authors (Adis and Righi 1989) believe that the temporary aboveground habitat could be a survival strategy in response to seasonal soil flooding. This behavior has been
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TABLE 2. Relative abundance by number and biomass of epigeic earthworms in bromeliads from Puerto Rico (Neotrigaster yukiyui and Trigaster complutensis) and Dominica (Eutrigaster sporadonephra), and other major litter processors Puerto Rico
Tabonuco Mid-elevation Cloud forest
Dominica
Earthworms
Isopoda
Diplopoda
Earthworms
Isopoda
Diplopoda
*0.1 (2)
