Comparing the Invertebrate Communities and the Decomposition Dynamics Between Dead Native and Non-Native Trees in a Seasonal Everglades Wetland
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Environmental Entomology, 50(5), 2021, 1056–1062
doi: 10.1093/ee/nvab057
Advance Access Publication Date: 24 June 2021
Research
Biological Control - Weeds
Comparing the Invertebrate Communities and the
Decomposition Dynamics Between Dead Native and
Non-Native Trees in a Seasonal Everglades Wetland
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Philip W. Tipping,1,5, Melissa R. Martin,2 Min B. Rayamajhi,1 Paul D. Pratt,3 and
Lyn A. Gettys4
1
USDA-ARS Invasive Plant Research Laboratory, Davie, FL, USA, 2USDA-NRCS, Washington, DC, USA, 3USDA-ARS Invasive
Species and Pollinator Health, Albany, CA, USA, 4Department of Agronomy, University of Florida, Ft. Lauderdale, FL, USA, and
5
Corresponding author, e-mail: philiptipping@gmail.com
Subject Editor: Raghu Sathyamurthy
Received 30 March 2021; Editorial decision 18 May 2021
Abstract
A 6-year time-series study in the Western Everglades region of Florida, United States examined the influence of
woody debris from two tree species on invertebrate richness, abundance, and diversity, as well as tree debris
mass loss, fragmentation, and residence time. Samples of decomposing fine woody debris and coarse woody
debris (CWD) from non-native Melaleuca quinquenervia (Cav.) Blake and native Pinus elliottii Englem trees
were removed from a field site every six months and processed to capture data on biotic and abiotic variables.
Invertebrates found within debris were identified to family. A total of 61,985 individual invertebrates from three
classes, 17 orders, and 95 families were identified from all debris. Although both tree species supported similar
richness and diversity of invertebrates, abundance was greater in P. elliottii CWD compared with M. quinquenervia.
Mass loss and fragmentation of debris were more rapid in M. quinquenervia fine woody debris with no differences
between species for CWD. Although M. quinquenervia CWD supported fewer invertebrates than P. elliottii, overall
the exotic tree provided a similar resource during the decomposition phase as the native P. elliottii suggesting that,
unlike when it is alive, its decomposing presence had a minimal impact on invertebrate food webs. Land managers
should consider specific intervals between herbicide applications and controlled burns to decrease the magnitude
of fires in areas where a significant portion of the fuel load consists of dead M. quinquenervia, knowing that the
decomposing trees are providing significant resources for invertebrate communities in the meantime.
Key words: decomposer communities, Woody debris, invertebrate diversity, fragmentation, invasive species
Plant invasions by non-native species can pose serious challenges to and nutrient dynamics associated with invasive plants have been
the integrity of natural and managed ecosystems by modifying the conducted with nonwoody plant materials, primarily leaf litter, to
basic ecosystem structure and the functions of communities including examine how their influence may feedback to soil processes (Hobbie
reducing producer diversity, simplifying consumer food webs, and 2015; Martin et al. 2010). Less well studied are the postmortem im-
altering the rates of nutrient cycling (Ehrenfeld 2003; Gerber et al. pacts of woody debris from non-native trees, including the nutrient
2008; Powell et al. 2011). These landscape-level impacts may con- pools associated with an individual tree as it decomposes and its
tinue after non-native species are killed by management efforts when resources are dispersed, as well as the physical effects of the woody
large amounts of plant debris, especially woody plant debris, are left structure itself on habitat conditions for other species over extended
to decompose in-situ. Although the main process behind decompos- periods (Franklin et al. 1987).
ition is the loss of organic matter through respiration by micro-or- Insects are among the most important of the soil meso- and mac-
ganisms, invertebrates play a pivotal role in transforming organically rofauna involved in the decomposition of woody materials, espe-
bound elements into bioavailable nutrients (Chambers et al. 2001; cially those in the Coleoptera and Isoptera during the initial phases
Mackensen et al. 2003). Most studies on the decomposition rates of decomposition (Edmonds and Eglitis 1989). During later phases
Published by Oxford University Press on behalf of Entomological Society of America 2021. This work is written
by (a) US Government employee(s) and is in the public domain in the US.
1056Environmental Entomology, 2021, Vol. 50, No. 5 1057
of decomposition, invertebrates like mites and collembolans become woody debris for this study. Based on height, the age of the P. elliottii
increasingly important because their mouthparts are capable of frag- trees was estimated to be between 15 and 20 yr (Bennett 1963). The
menting organic matter while feeding on the microflora adhering lack of field-based studies on the growth rates of M. quinquenervia
to the detritus (Seastedt 1984). Further fragmentation creates new prevented a reliable estimate of age in this study.
surface areas for microbial colonization which may influence decom-
position rates (Elkins and Whitford 1982). Sampling Methods
The objective of this study was to compare the decomposition The experiment was designed as a time-series and was conducted
of woody debris from a non-native and a native tree by examining from 14 March 2006 through 17 April 2012 in a 3.5 ha plot that was
the richness, diversity, and abundance of common invertebrate taxa centered at 26.104 N and 81.635 W in Picayune Strand. Five mature
found over time. In addition, some biogeochemical aspects of de- wind thrown trees from each species were selected without bias and
composition were examined to compare differences in mass loss, cut into 25 cm long logs and branches to fit coarse woody debris
fragmentation, and residence time between tree species. (CWD [>10 cm diameter]) and fine woody debris (FWD [1–10 cm
diameter]) size classes (Nordén et al. 2004). Nontapering debris
was selected with uniform diameters along the entire length and the
Methods
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diameter was measured at the midpoint to estimate volume based
Site Description on the volumetric calculation for a cylinder (Table 1). All debris was
The study site was located in the Belle Meade Tract of the Picayune labeled with a tag that identified the tree species, debris size class,
Strand State Forest in Collier County, Florida, United States. This site, block, and date to be sampled. The site referred to two locations
area consists of nearly level, poorly drained, low fertility soils which that differed slightly in elevation (1058 Environmental Entomology, 2021, Vol. 50, No. 5
Data Analysis Results
Family abundance data were analyzed as a multivariate data set
Invertebrate Abundance and Diversity
using PAST v3.25 software with 12 sample dates, two tree species,
A total of 61,985 individual invertebrates from three classes, 17 or-
two debris sizes, two sites, and five replications (Hammer et al.
ders, and 95 families were tallied from all tree species and debris
2001). Sample-based rarefaction curves and their confidence inter-
sizes during this study using keys found in Triplehorn and Johnson
vals were calculated and compared for the number of invertebrate
(2005). Sample-based rarefaction found significantly greater family
families found in M. quinquenervia and P. elliottii FWD and CWD
richness in P. elliotti CWD (Fig. 2). This outcome largely supported
(Colwell et al. 2004). A two-way permutational multivariate analysis
the PERMANOVA analysis showing that the richness of inverte-
of variance (PERMANOVA) was used to compare differences in in-
brates was influenced by debris size but not by tree species (Table
vertebrate richness between tree species and over time (Anderson
2). The SHE analysis noted similar patterns across species and debris
2001). An analysis of similarity percentages (SIMPER) was calcu-
sizes and showed an initial sharp increase in richness (LnS) followed
lated for each tree species to identify those families that were most
by a leveling off of the curve as more families were accounted for by
responsible for the observed patterns by disaggregating the Bray-
repeated sampling. Evenness (LnE) declined over the same period
Curtis similarities between samples (Clarke 1993). A SHE analysis
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while H remained constant, a pattern that can be explained by an
for biofacies, or groups of families in this study, was performed using
increase in the proportion of the abundant families over time (Fig
the time (sample) rather than an environmental gradient to examine
3). SIMPER analysis supported this interpretation by showing that
any changes in family richness (S), evenness (E), and the pattern of
about 75% of all samples consisting of individuals from just three
change provided by the information function (H) (Buzas and Hayek
families, with 12 families comprising 90% of all sampled inverte-
1998). In this analysis, the quantities of S, H, and E were computed
brates (Table 3). Although SHE analysis showed similar patterns
as the samples were accumulated. Any departures from known ex-
among species and debris size for richness and evenness across time,
pected patterns can provide evidence of changes in invertebrate as-
N (abundance) was consistently higher for P. elliottii (Fig. 3).
semblages over time that may be related to temporal factors like
ANOVA found that diversity was significantly (P = 0.05) influ-
decomposition or water stage.
enced by debris size only (F1,47 = 11.46, P = 0.001); there was no
Diversity, woody debris mass loss, and fragmentation were first
influence of tree species (F1,47 = 3.11, P = 0.08) nor any interaction.
analyzed over time using PROC AUTOREG (SAS Institute 2009) for
There was a first-order positive autocorrelation for diversity
the presence of nonindependent errors often found in time-series data
(d = 1.41, n = 45) that was eliminated using an AR(1) covariance
and the Durbin-Watson d-statistic was used to test for the existence
model. The response surface model indicated that only a linear
of first- or multi-order autoregressive processes that might indicate
term was needed (F2,5 = 4.62, P = 0.01) and that all terms with time
the residuals were correlated (Freund and Littell 2000; Durbin and
Watson 1951). If correlated errors were detected, then various mod-
els were examined and adopted to eliminate autocorrelation. The
autoregressive parameter estimates were modified using Yule-Walker
equations to estimate the autocovariances to obtain the generalized
least squares estimates. The first-order autoregressive or AR(1) co-
variance model adequately described any correlations found in the
observations over time when they were detected. The principal
measure of diversity used at the family level was Shannon’s index of
diversity which incorporates richness and evenness (Shannon 1948).
A two-factor ANOVA was used to examine the influence of tree spe-
cies and debris size on mean diversity (SAS Institute 2009). A quad-
ratic response surface model was utilized to examine the relationship
between mean diversity with the variables time (sample) and water
stage (Freund and Littell 2000).
Analysis of covariance was used to compare mass loss and frag-
mentation of woody debris between species by determining if their
slopes or Y-intercepts differed over time. The residence time of
debris, or the time required for the debris to decompose completely, Fig. 2. Schematic representation of individual rarefaction curves for
was estimated using simple linear regression of mass loss data. M. quinquenervia and P. elliottii FWC and CWD over a six-year period.
Table 1. Mean (± SE) initial metrics of fine woody debris (FWD) and coarse woody debris (CWD) of M. quinquenervia and P. elliottii
Variable Species n FWD t n CWD t
Biomass (g) M. quinquenervia 130 100.6 ± 3.95 1.56 130 2574.7 ± 117.3 1.11
P. elliottii 128 87.1 ± 6.2 130 2768.9 ± 129.2
Length (cm) M. quinquenervia 130 25.0 ± 0.06 2.75** 130 25.0 ± 0.07 2.13*
P. elliottii 130 25.3 ± 0.09 130 24.7 ± 0.06
Diameter (cm) M. quinquenervia 130 3.3 ± 0.06 1.67 130 15.9 ± 0.34 1.51
P. elliottii 130 3.1 ± 0.10 130 15.2 ± 0.33
*,**P = 0.05, 0.001, respectively, with two-sample t-testing of variables between tree species within debris sizes.Environmental Entomology, 2021, Vol. 50, No. 5 1059
Table 2. PERMANOVA partitioning and analysis of invertebrate assemblages (95 taxa) from M. quinquenervia and P. elliottii FWD and CWD,
based on Bray-Curtis dissimilarities
Source df SS MS Pseudo F p
Tree species 1 0.16446 0.16446 0.4807 0.908
Debris size 1 1.3871 1.3871 4.055 0.0004
Tree species × Debris size 1 0.226 0.226 0.661 0.575
Residual 44 15.051 0.34207
Total 47
Pseudo F statistics were calculated for each term using direct analogs to univariate expectations of mean squares; p-values were obtained using 9,999 permu-
tations under a reduced model.
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Fig. 3. Representation of SHE analysis of invertebrate family S (richness), H (information), and E (evenness) from samples taken from M. quinquenervia (Mq)
and P. elliottii (Pe) FWD and CWD over six years.
as a factor could be omitted from the model (F3,5 = 1.45, P = 0.24). Mass Loss, Fragmentation, and Residence Time
Simple linear regression thus found that higher water stages re- There was a first-order autocorrelation in the mass loss data for
sulted in decreased diversity, an outcome that supported patterns FWD (d = 1.6, n = 114) that disappeared using an AR(1) covariance
evident in the SHE analysis where fewer individuals were collected model. Melaleuca quinquenervia FWD decomposed at a faster rate
between sample dates that roughly corresponded to higher water than P. elliottii (F12, 169 = 2.75, P = 0.002) while there was no differ-
stages (Fig. 3). ence in the rate of decomposition for CWD (F12, 176 = 1.56, P = 0.1)1060 Environmental Entomology, 2021, Vol. 50, No. 5
Table 3. Summary of SIMPER results for tree species: average dissimilarities, contribution (%), cumulative total (%) of contributions (90%
cutoff), and means for the invertebrate families most responsible for the distinction between tree species
Taxon Dissimilarity Contribution Cumulative Mean (Mq)1 Mean (Pe)
Isotomidae 28.11 36.25 36.25 43.2 75.3
Rhinotermitidae 15.93 20.55 56.79 22.8 64.9
Acarina 13.52 17.44 74.23 26.4 19.0
Formicidae 2.86 3.69 77.92 1.38 2.37
Psocidae 2.81 3.63 81.55 1.79 2.5
Sciaridae 1.58 2.04 83.60 1.32 1.59
Spirobolidae 1.25 1.61 85.21 1.12 1.46
Cecidomyiidae 1.21 1.56 86.78 1.01 0.77
Staphylinidae 0.84 1.09 87.87 2.00 0.68
Anobiidae 0.82 1.06 88.93 0.42 0.30
Chironomidae 0.77 0.99 89.93 0.57 0.21
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Mycetophilidae 0.69 0.89 90.83 0.96 0.11
1
Mq = M. quinquenervia, Pe = P. elliottii.
(Fig. 4). Fragmentation was influenced by tree species with FWD (F12, smaller woody debris is composed primarily of relatively labile sap-
171
= 2.84, P = 0.001) but not with CWD (F12, 178, P = 0.22) (Fig. 5). wood that contains a higher proportion of sugars, whereas a large
Neither fragmentation of FWD nor CWD exhibited autocorrelation. portion of mature tree mass or CWD is recalcitrant heartwood that is
On average, the residence times for FWD were 9.4 and 12.8 yr for denser, often contains complex compounds, and has a lower nutrient
M. quinquenervia and P. elliottii, respectively. Residence times for content (Grubb and Edwards 1982; Sellin 1994; Meerts 2002). Some
CWD were 11.3 yr for M. quinquenervia and 10.3 yr for P. elliottii. of these complex compounds consist of fungi- or insect-toxic extrac-
These values are estimates based on regression equations over 6 yr tives which may inhibit the invertebrates that play an important role
and thus should be interpreted with caution because the exponential in determining log decomposition rates (Harmon et al. 1986; Idol
model of decomposition is only a rough approximation of the pat- et al. 2001). Normally, higher rates of decomposition decrease wood
tern of decline with time (Chapin et al. 2002). density and increase the moisture content of debris. These more fa-
vorable abiotic conditions may support larger microbial and inverte-
brate communities thereby promoting faster rates of decomposition.
Discussion This pattern is likely responsible for the increase in mass loss and
Previous studies have shown that the establishment and expansion fragmentation of both the native and non-native debris over time.
of M. quinquenervia alter the structure and function of invaded However, the beneficial effects of the fragmentation process may
ecosystems, including relative rates of litter decomposition (Martin have been muted by the periodic seasonal inundation of the debris.
et al. 2009; Martin et al. 2010). While integrated management ef- In addition, site inundation and the resulting reduction in oxygen
forts have significantly reduced the invasiveness and limited the availability for microbial and invertebrate communities likely had
landscape level footprint of this non-native tree, less is known about a disproportionate effect on decomposition rates of the nonfloat-
post-treatment ecosystem functions that may influence the ability of ing CWD compared with floating FWD (Fig. 1) (Rayner and Boddy
managed and natural areas to recover. In this study, although family 1988; Progar et al. 2000).
invertebrate richness and diversity were not reduced in non-native Invertebrates and their interactions with woody debris are crit-
tree debris throughout the study, overall invertebrate abundance was ical to maintaining nutrient cycles within communities (Swift et al.
lower which suggests that a resource difference existed between the 1979). The inclusion of woody debris with other plant biomass pro-
tree species. This has implications for the food webs in these commu- vides a broader picture of how these combined plant components
nities because the decomposition process forms the trophic base that may influence nutrient cycles in this system. For example, M. quin-
supports the soil fauna (Butterfield 1999) and it is the detritivores quenervia litter decomposes faster than does litter from natives like
and mycophages, such as Collembola and mites, that form the main P. elliottii and, in conjunction with once higher biomass production,
prey of many spider and beetle species in these webs (Hengeveld may have changed nutrient cycles to favor its persistence (Martin
1980; Buse and Good 1993). Any modifications in consumer abun- et al. 2010). This has changed in the past decade with the introduc-
dance will likely be reflected at higher trophic levels. Although diver- tion and establishment of several monophagous herbivores as part of
sity was calculated using families, data from aquatic systems have a classical biological control program that has limited both litterfall
demonstrated good agreement between family level and species-level and seed production (Tipping et al. 2012).
diversity indices; the lack of family level differences in diversity in The residence times of debris also have implications for follow-on
this study does not imply that such differences are absent at the spe- management, especially with the use of fire. Land managers may
cies level (Hughes 1978; Hoback et al. 1999). consider setting specific intervals between herbicide applications and
Debris size was an important determinate in the rates of decom- controlled burns to decrease the magnitude of fires in areas where
position in this study, confirming the frequently observed size effect a significant portion of the fuel load consists of dead M. quinquen-
whereby the decomposition rate is inversely related to log diameter ervia. Residence time for M. quinquenervia killed by herbicides is
(Mackensen et al. 2003). This phenomenon may be explained by likely to be longer because the resulting snags will likely decompose
a lower surface: volume ratio which can lower the rates of gas ex- more slowly than the downed and cut up trees in this study (Harmon
change (Abbott and Crossley 1982). Another explanation is that et al. 1986; Song et al. 2017).Environmental Entomology, 2021, Vol. 50, No. 5 1061
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Fig. 4. Relationship between the mean percentage of debris mass loss and Fig. 5. Relationship between mean percentage of debris volume
months of field weathering for M. quinquenervia and P. elliottii with FWD (A) (fragmentation) and months of field weathering for P. elliottii (A) and
and CWD (B). M. quinquenervia (B) with FWD and CWD.
Quantifying ecosystem impacts of invasion by non-native plants Acknowledgments
requires not only measuring the influence of living plants on natural We thank D. Fitzgerald, J. Leidi, K. Nimmo, R. Moscat, E. Pokorny, J. Scoles,
communities but also their postmortem legacy after plants die natur- C. Silvers, and M. Smart for their assistance in processing samples.
ally or are killed by management. In this study, differences between
tree species were minimal, namely that M. quinquenervia CWD sup-
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