BIOTROPICA 47(2): 201–207 2015
10.1111/btp.12204
The Stability of Invertebrate Communities in Bromeliad Phytotelmata in a Rain Forest Subject to Hurricanes Michael J. Richardson1,2,4, Barbara A. Richardson1,2, and Diane S. Srivastava3 1
165 Braid Road, Edinburgh EH10 6JE, U.K.
2
Luquillo LTER, Institute for Tropical Ecosystem Studies, College of Natural Sciences, University of Puerto Rico at Rio Piedras, P.O. Box 70377, San Juan, Puerto Rico, 00936-8377, U.S.A.
3
Department of Zoology and Biodiversity Research Centre, University of British Columbia, 6270 University Blvd, Vancouver, BC, V6T 1Z4, Canada
ABSTRACT Communities of invertebrate animals in lower canopy and saxicolous tank bromeliads, originally studied in 1993–1997, were resampled along an elevational gradient in tabonuco, palo colorado, and dwarf or cloud forest in Puerto Rico in 2010. These Puerto Rican montane rain forests were impacted strongly by hurricanes in 1989 and 1998, so the surveys in the 1990s represented 4–8 yr of post-hurricane recovery, whereas our recent survey represents 12 yr of post-hurricane recovery. At most elevations, species diversity, both within individual bromeliads and at the forest scale, declined between the 1990s and 2010. This decline in diversity between decades is associated with reductions in bromeliad density as the canopy progressively closed during recovery from hurricane damage. The observed decline in alpha and gamma diversity appears to have involved the loss of rarer species, as might be expected from standard metapopulation theory. By contrast, the most common species were remarkably stable in abundance, composition, and frequency of occurrence over the two decades. In the lowermost tabonuco forest, two endemic bromeliad specialists, restricted to bromeliads for their entire life cycle, were not found on resampling. This study also demonstrates that, at least in Puerto Rico, sets of ten plants from each forest were sufficient to monitor bromeliad invertebrate populations and their diversity over time. Abstract in Spanish is available in the online version of this article. Key words: community change; diversity; Guzmania; habitat loss; habitat monitoring; tank bromeliad; Vriesea.
WATER AND LITTER IMPOUNDED BY THE ROSETTES OF TANK BROMELIADS support terrestrial and aquatic macroinvertebrates, many of which are unique to this habitat (Frank & Lounibos 2009). The macroinvertebrate food web is supported by inputs of leaf litter and, sometimes, endogenous primary production (Srivastava 2006, Brouard et al. 2011). Detritivores also make nutrients available to the bromeliad plants by absorption through their leaf bases (Benzing 1986, Ngai & Srivastava 2006). Early research on bromeliad fauna was primarily taxonomic (Picado 1913, Laessle 1961, Frank 1983). More recently, the microcosms have been used to test ecological theory about the structure of communities and food webs (Cotgreave et al. 1993, Srivastava et al. 2008, Farjalla et al. 2012, Dezerald et al. 2013). Many organisms are bromeliad specialists not found in other habitats, but there is little evidence of species-specific associations between different bromeliad species and their fauna once the microhabitat is accounted for (Benzing 1990, Marino et al. 2012). It would seem that bromeliads generally fulfill a common habitat requirement for widespread and largely detritivorous species. Vertical distribution appears to be unimportant, at least in lower canReceived 29 July 2014; revision accepted 25 November 2014. 4
Corresponding author; e-mail:
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ª 2015 The Association for Tropical Biology and Conservation
opy bromeliads, as no differences in animal species assemblages were found between those from higher in the canopy (4–12 m) and from low-level saxicolous and epiphytic plants (< 2 m) (Richardson et al. 2000). As bromeliads are discrete, usually abundant units, and their complete animal communities can be obtained, they are ideal subjects for replicated and comparative quantitative studies. Until the studies of Richardson (1999) and Richardson et al. (2000), however, there appeared to have been no detailed quantitative studies of such microcosms. They studied bromeliad animal communities over 4 yr (1993–1997) from three forest types along an elevational gradient in the Luquillo Experimental Forest (LEF), a moist tropical forest in Puerto Rico: tabonuco forest < 600 m, palo colorado forest 600–900 m, dwarf forest > 900 m. The work began 4 yr after 1989’s Hurricane Hugo. Since Hurricane Georges in 1998, the LEF has been in a period of recovery, with seedling recruitment, understorey growth, and then suppression with canopy closure (Comita et al. 2009). Caribbean forests are shaped by hurricanes that cause structural damage to the canopy through defoliation, branch and tree falls, with consequential changes in light regime, microclimate, and increased heterogeneity in the understorey (Brokaw et al. 2012). Changes in light regime are necessarily cyclical, as pioneers and other tree species fill gaps and the remaining canopy recovers 201
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between successive hurricanes, resulting in the suppression of the understorey. There is also evidence of generally increasing liana abundance and biomass in New World forests due to increasing forest disturbance, fragmentation, and elevated atmospheric CO2. This increase in lianas can add to shading and result in decreased tree diversity, recruitment, growth, and survival (Schnitzer & Bongers 2011) and could also reduce understorey bromeliad density. In 1989, the LEF in Puerto Rico was severely damaged by Hurricane Hugo and again by Hurricane Georges in 1998. The hurricanes noticeably affected bromeliad distribution and density in some areas, and the opportunity has been taken to study the long-term effects on bromeliad invertebrate communities. Bromeliad plant populations in the lowermost canopy and forest floor can be directly reduced by hurricanes as supporting branches fall to the ground. They can also be reduced indirectly over the longer term by changes in the light regime from the stripping of leaves and vines and branch loss from the canopy. Bromeliads, even shade-tolerant ones such as Guzmania lingulata, were not regarded as true shade plants by Pittendrigh (1948), but rather as plants able to tolerate high light levels but requiring the higher humidity of the lower canopy. This assertion was substantiated in physiological experiments by Griffiths and Maxwell (1999) that demonstrated the ubiquitous capacity of bromeliads to tolerate high light intensity. The effect of post-hurricane forest recovery on the bromeliad fauna is unknown. On the one hand, any change to the forest structure affecting understorey bromeliad density could affect their specialized invertebrate communities because of loss or isolation of suitable habitat. On the other hand, because the aquatic and moist litter habitat in bromeliads buffers any changes in the forest microclimate, invertebrate communities in bromeliads may be predicted to remain stable despite changes in the forest. We tested the stability of bromeliad communities over time by resampling the LEF bromeliad communities in 2010 and identifying changes in the intervening 13–16 yr.
STUDY SITE The Luquillo Experimental Forest is part of El Yunque National Forest, in hurricane-prone northeastern Puerto Rico, and is a U.S. Long Term Ecological Research (LTER) site. The steep topographic gradient of the Luquillo Mountains (sea level to 1000 m asl in 8 km) produces landscape-scale variability in the local climate, abiotic characteristics, and disturbance regime. Temperature decreases and precipitation increases toward the summits, which are often covered in orographic cloud. Along the gradient, three major forest types occur: tabonuco forest, with Dacryodes excelsa dominant and canopy height
