Effects of fire severity on the composition and functional traits of litter-dwelling macroinvertebrates in a temperate forest

Forest Ecology and Management 434 (2019) 279–288

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Effects of fire severity on the composition and functional traits of litterdwelling macroinvertebrates in a temperate forest Sebastian Buckinghama,b, Nick Murphyb, Heloise Gibbb, a b

T

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College of Science, Engineering and Health, RMIT University, Melbourne, Vic 3001, Australia Research Centre for Future Landscapes and Department of Ecology, Evolution and the Environment, La Trobe University, Melbourne, VIC 3086, Australia

A R T I C LE I N FO

A B S T R A C T

Keywords: Detritivore Predator Body size Extinction Dispersal

High severity fires are likely to become more prevalent with global climate change, so it is critical that we understand their effects on forest ecosystems. Leaf litter dependent fauna are likely to be particularly vulnerable to habitat loss resulting from fire, which often destroys their leaf litter habitat. We hypothesised that, as fire severity increased: (1) richness and abundance of macroinvertebrate litter fauna would decline; (2) species composition would change; and (3) species responses would depend on morphological and trophic traits, with proportions of larger, winged and predatory species increasing with fire severity. To test the effects of fire severity on the composition and functional traits of litter-dwelling macroinvertebrates, we collected macroinvertebrates using litterbags and standardised hand searches of logs at unburnt, low severity (ground burnt) and high severity (crown burnt) burnt eucalyptus forests (n = 7) in south eastern Australia, three years after fire. Litter-dwelling macroinvertebrates were larger, less abundant and less species-rich at high severity burnt than unburnt sites and species composition differed from unburnt and low severity burnt sites. Fire severity did not affect the proportion of winged species or individuals. Thus, we suggest small bodied species may struggle to recolonize through limited dispersal ability or may be limited by the drier post-fire environment. Increases in large scale, high severity fires may therefore result in assemblages dominated by larger macroinvertebrate species, but will also be associated with lower species richness.

1. Introduction Fire transforms ecosystems by removing biomass and altering physical and biological conditions. Of general concern is the loss of habitat complexity and other organic legacies that take years to develop after incineration results in the local extirpation of fauna (Bowman et al., 2009; Chapin et al., 2012). Fire varies in frequency, extent and severity (Gill and McCarthy, 1998). While the effects of fire frequency and time since fire on species composition are well studied (Turner et al., 1997; Saint-Germain et al., 2005; Moretti et al., 2006; Pryke and Samways, 2012; Kwok and Eldridge, 2015), the effects of fire severity and extent are less well known (Wikars and Schimmel, 2001; Smucker et al., 2005; Rodrigo et al., 2008; Malmström, 2010). Here, we focus on the effects of fire severity, which is expressed as the amount of fuel burnt in a fire (Keeley, 2009). High severity wildfires often result in complete incineration of habitat (Certini, 2005; Cawley et al., 2017) and typically occur over large spatial extents (Macias Fauria and Johnson, 2008). High severity forest fires are likely to become more common in both temperate and tropical climates, globally, as extended hot and dry

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weather events become more frequent, facilitating uncontrolled wildfires (Johnson et al., 2001). High severity fires have the potential to cause local extinctions (Wikars and Schimmel, 2001; Rodrigo et al., 2008). If sufficient refuges remain during fire, then local populations will survive (Robinson et al., 2013). However if refuges are lost, as is likely during severe fires, then local populations may become extinct and successful recolonization would then be required to ensure persistence in the landscape (Rodrigo et al., 2008; Fattorini, 2010). Populations must also survive post-fire changes in food resources, shelter availability and species interactions (e.g. predation and competition) (Whelan, 1995). Low severity fires are likely to be more heterogeneous and provide more refuges than high severity fires (York, 1999; Malmström, 2010; Gongalsky et al., 2012; Zaitsev et al., 2014). In contrast, in forest ecosystems, severe fires incinerate not only leaves in the tree canopy and fine fuels on the forest floor, but also other biological legacies, such as logs, that may have long-term impacts on the persistence of organisms (Franklin et al., 2000; Gandhi et al., 2001; Banks et al., 2011). Knowledge of the effects of fire severity on vertebrate fauna and habitat is scant (Bassett et al.,

Corresponding author. E-mail address: [email protected] (H. Gibb).

https://doi.org/10.1016/j.foreco.2018.12.030 Received 7 September 2018; Received in revised form 14 December 2018; Accepted 16 December 2018 0378-1127/ © 2018 Elsevier B.V. All rights reserved.

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daily minimum winter temperature was 3.8 °C. Sites were located in damp sclerophyll forest in gullies dominated by messmate stringybark (Eucalyptus obliqua), around 25 m tall with a dense midstorey of tree fern (Dicksonia antarctica) and hazel pomaderris (Pomaderris aspera). These damp gullies are typically surrounded by dry sclerophyll forest with an open midstorey. The 2009 Kilmore East-Murrindindi fire was ignited on February 9th, 2009. Initially severe weather conditions supported high severity crown fires, but wind speed and fire flame height later declined, resulting in a burn area of over 228,000 ha (Teague et al., 2010). Sites were selected within the border of this fire in three fire severity classes with seven replicates (a total of 21 sites) (Fig. 1). Fire severities were classified as follows: (1) Crown burnt (high severity), referring to the incineration of all leaves in the tree crown and midstorey, leaf litter, humus, and logs; (2) Ground burnt (low severity), litter layer and underlying humus layer incinerated and/or charred; logs typically charred where exposed but sometimes wholly burnt; the shrub and ground layer vegetation, but not the tree crown, is typically burnt; and (3) Unburnt, referring to sites not burnt or directly affected by fire in 2009. All sites were unburnt and unaffected by logging for at least 20 years prior to 2009. Sites were interspersed over an area of 30 by 50 km and separated by a minimum distance of 150 m and sites of the same fire severity were separated by a minimum distance of 1.15 km.

2015), but even less is known about responses of invertebrates, particularly those that dwell in the flammable litter layers (Wikars and Schimmel, 2001; Rodrigo et al., 2008). Litter-dwelling macroinvertebrates are responsible for between 13% (coniferous forest) and 47% (humid grasslands) of litter decomposition in biomes worldwide (Garcia-Palacios et al., 2013; Buckingham et al., 2015; Ossola et al., 2016; Ossola and Nyman, 2017) and invertebrates are key contributors to biodiversity (Wilson 1987). A loss of detritivorous invertebrates and a changed biophysical environment caused by fire can reduce rates of leaf litter decomposition (Brennan et al., 2009). Macroinvertebrate detritivores, such as millipedes (Diplopoda), woodlice (Isopoda) and nematoceran fly larvae (Diptera: Nematocera) (Zimmer, 2002; Heemsbergen et al., 2004; Kitz et al., 2015), break down leaf litter by fragmenting fresh intact leaves or consuming microbially conditioned leaves and re-ingesting leaf material. However, not all litter-dwelling macroinvertebrates are detritivores, with assemblages including true fungivores, such as fungus gnats (Diptera: Sciaridae) (Kitz et al., 2015), and predators, such as spiders (Araneae), centipedes (Chilopoda) and ground beetles (Coleoptera: Carabidae), regulating assemblages of other organisms. Due to the key role that this fauna plays in forest ecosystems by driving flows of matter and energy through the food web and recycling nutrients, it is critical that we understand how it is influenced by environmental stressors, such as fire. While previous studies have emphasised effects of fire on taxa, recent work suggests a focus on functional traits may provide greater insights into the mechanisms driving ecosystem change and recovery (McGill et al., 2006; Langlands et al., 2011; Podgaiski et al., 2013; Buckingham et al., 2015). In particular, functional traits related to post-fire persistence are likely to be critical in determining species composition following a severe fire. For example, species with large body size are more common following high severity burns, probably because they are better able to move and resist desiccation (Buckingham et al., 2015); winged species are more prevalent in ephemeral habitats (Mclachlan, 1985; Williams, 1996), such as those resulting from fire; and large-scale disturbances have been shown to alter trophic structure and change ecological functions, e.g., decomposition (Thompson et al., 2012). We tested the effects of fire severity on litter macroinvertebrate assemblages in eucalyptus forests, three years after severe fires. We hypothesized that: (1) richness and abundance of macroinvertebrate litter fauna would decline with increasing fire severity; (2) species composition would change with fire severity; and (3) that the response of species to fire severity would depend on species morphological and trophic traits. The way in which species traits responded was expected to indicate whether assemblage recovery was most limited by dispersal ability, physiological tolerance or food availability (Fig. 1). If active dispersal following local extinction best explains the change in species composition, then post-fire assemblages should include increasing numbers of large and winged species as fire severity increases. If greater desiccation and temperature tolerance best explains species composition, then only body size would be expected to increase with increasing fire severity. However, if food resources are the primary determinant of species composition, we would expect increasing fire severity to be associated with an increasing proportion of predators, which do not depend directly on litter. (See Fig. 2)

2.2. Macroinvertebrates To test the effects of fire severity on litter-dwelling macroinvertebrates, we sampled using litterbags and log sampling. Leaf fall starts in late spring and is at a maximum in summer and early autumn (Ashton, 1975; Attiwill, 1979); therefore litterbags were placed out in spring (October 2011) to coincide with natural pulse of unweathered leaves that appears on the forest floor at this time. Litter was sourced from a single unburnt site and we placed litterbags directly on the soil and covered them with leaf litter at each site for the first experiment. Litter bags were 180 mm × 180 mm, with a mesh width of 8 mm and contained 10 g of dried E. obliqua leaves (collected green). Green leaves make up around 10% of total leaf fall in E. obliqua forest (Attiwill, 1979), so are a representative substrate. Ten litter bags were placed at 3 m intervals along a 30 m transect at each site. We collected macroinvertebrates in autumn (March) 2012 to avoid both extreme hot dry summer conditions and cold wet winter conditions and thereby be better representative of fauna present (Ashton, 1975). Litter was placed in Tullgren funnels for 48 hrs to extract living animals. Earlier tests using 10 g of wet leaf litter collected from the field confirmed that extraction of all living animals was achieved over a 2 day period. We also conducted active searches under logs. Because some litterdwelling macroinvertebrates are known to temporarily utilize habitat under bark and rotten woody debris, ten log subsamples were located as close as possible to the 10 corresponding litterbags. Each subsample was a 20 cm × 100 cm area of log. Here, the collection was restricted to wingless detritivores that were known to be poor dispersers or vulnerable to desiccation, i.e. millipedes and crustaceans, because they were presumed to be the most responsive to fire severity (due to their reliance on leaf litter as a food source and their poor dispersal ability). To test the effects of fire severity on the composition of macroinvertebrates, we identified all specimens to family and, where possible, determined their trophic status (Holloway et al., 1987; CSIRO, 1991; Coleman et al., 2004; Booth et al., 1990) and whether species were apterous, brachypterous or macropterous as adults. A limited number of families could not be confidently identified due to a lack of specialised knowledge and were given a higher taxonomic level designation: moths (Lepidoptera), harvestmen (Opiliones), spiders (Araneae), predaceous/ scavenging flies (Brachycera), true bugs (Hemiptera); and earthworms (Annelida). The body length of all individuals greater than 2 mm was measured and used for analysis of body size because they included all the

2. Methods 2.1. Study sites We tested the effects of fire severity on macroinvertebrate assemblages in forests located within the 2009 Kilmore East-Murrindindi fire complex, in the foothills of the Great Dividing Range, Victoria, southeast Australia (37°34′S, 145°30′E) (Fig. 1). The climate is temperate with a mean annual rainfall of 1373 mm recorded at 595 m a.s.l. The mean daily maximum summer temperature was 23.2 °C, while the mean 280

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Traits:

body size

wing presence

trophic role

Increasing % predators

Food availability

Increasing % winged

Physiological tolerance

Increasing body size

Hypothesised mechanisms

Dispersal ability

***

trend

trend

Findings of this study

Increasing fire severity Fig. 1. Predicted status of species traits (body size, wing presence and trophic role) as fire severity increases, depending on the key mechanisms (dispersal, physiological tolerance and food availability) through which trait-based filtering of assemblages functions three years after fire and findings from this study. Trends were in the expected direction for all traits, but were only significant for body size, which was predicted to increase through all three mechanisms.

litterbag, making a total of (9 × 20) or 180 measurements per site during the single collection period in autumn (March) 2012. We measured the percentage cover of ground, midstorey and canopy foliage. Midstorey and canopy foliage cover were estimated visually within a 2 m × 2 m quadrat. Percentage cover of ground foliage, leaf litter, bare ground and moss was estimated visually within a 30 cm × 30 cm quadrat directly adjacent to litterbags. Litter depth was measured at three points within each 30 cm × 30 cm quadrat. We also measured the distance of each litterbag to the nearest log of diameter greater than 10 cm. Moisture was measured with a meter CT-250 Cool Tech (Testequipment, Australia) inserted within the litterbag and relative humidity was recorded by placing a Kestrel 4500 Pocket Weather Tracker (Nielsen-Kellerman, U.S.A.) on the soil beneath each litter bag immediately after collection. We previously reported distinct differences in microhabitat variables among fire severity classes three years after fire (Buckingham et al., 2015): moss cover was greatest in crown burnt sites, while soil disturbance, principally caused by digging vertebrates, including the superb lyrebird (Menura novaehollandiae) and long-nosed bandicoot (Perameles nasuta), tended to be highest in unburnt sites.

functionally important fauna (principally larvae, but also adults) that ingest leaf litter (Coleman et al 2004). Microarthropods less than 2 mm (primarily Acarina and Collembola in this study) are principally microbivores or predators that feed on these fungivore/microbivores and represent a separate energy channel (Wardle, 2002). However, some microarthropods less than 2 mm were also potentially important consumers of leaf litter, principally box mites (Acarina: Philithridae) (Coleman et al., 2004). These were observed in the samples, but at very low numbers, often as singletons, and were assumed to play a minor functional role in the fragmentation of leaf material in this system. Ground beetle (Carabidae) larvae and spiders (Araneae) were excluded from analyses of dispersal ability because carabid adults exhibited both winged and wingless characters and could not be matched to larvae, whilst some species of spider disperse aerially by 'ballooning' (den Boer, 1990) (these taxa made up 3% of individuals collected). Beetles (Coleoptera) were identified to morphospecies and used to test specieslevel compositional responses to fire severity and associated microhabitat variables. We used both the richness and density data for coleopterans in calculations of total richness and abundance. Unlike moths and flies (Tipulidae, Chironomidae and Bibionidae), adult and larval Coleoptera presented sufficient morphological features to determine composition at a species level. This group is also species-rich, but is known to have variable trophic roles and dispersal ability (Didham et al., 1998; Driscoll and Weir, 2005; Gibb and Cunningham, 2010) and therefore provided an opportunity to examine species and trait responses on a finer taxonomic level.

2.4. Statistical analyses We used ordinary least squares (OLS) regression in the package MASS in R (R Development Core Team, 2013) to test the effect of fire severity (three categories: unburnt, low severity burn and high severity burn) and seven microhabitat variables on litter-dwelling macroinvertebrates, focussing on the following response variables: taxon richness, predator and non-predator abundance and mean body size, and Coleoptera species richness and abundance. Our initial nine microhabitat variables were reduced to seven for analysis because

2.3. Microhabitat parameters Nine microhabitat measurements were made twice for each 281

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Fig. 2. Study-site location and sampling design. Inset shows the location of the 2009 Kilmore-Murrindindi fire complex in Australia (top right). Main image shows the 21 sites in the three fire severity classes: Crown Burnt (high severity); Ground Burnt (low severity); and Unburnt. Background colours represent burn status; the grey region is beyond the extent of the fire.

fire severity on taxa and morphospecies for Coleoptera composition in litter bags using non-metric multidimensional scaling (NMDS) plots based on Bray-Curtis similarity (Primer software, version 6) (Clarke and Gorley, 2006).

moisture covaried with humidity (R2 = 0.52, F(1,19) = 22.3, P < 0.001) and litter cover had a negative covariance with bare soil (R2 = 0.44, F(1,19) = 16.45, P < 0.001). Non-predators included both macroinvertebrate detritivores and fungivores, e.g., fungus gnats (Sciaridae). We used the Bernoulli multiple trial method (Crawley, 2011) to test the effect of fire severity and seven microhabitat variables on the percentage of taxa with wings, predator taxon richness, predator taxon abundance and mean predator taxon size. The Bernoulli multiple trial method provides a better estimation of error when using percentages and specifies a binomial Generalised Linear Model (GLM) using the MASS package. An Akaike information Criterion (AIC) modelstepwise regression was used to decide on the best model. When we detected overdispersion by examining residual plots, we used a quasiGLM model, which precluded model selection (Venables and Ripley, 2002). We also tested the effects of burn severity on the minimum, maximum and median body size using ANOVA on R. Post-hoc Tukey's tests were conducted when the effect of fire severity was significant. We used Many Generalised Linear Model (ManyGLM) regressions to determine the effect of fire severity and seven microhabitat variables on the composition of litter-dwelling macroinvertebrates for taxa (in litter bags and logs) and Coleoptera species (in litter bags only). ManyGLM is a model-based multivariate approach available in the package mvabund on R (Warton, 2011; Wang et al., 2012; R Development Core Team, 2013). For ManyGLM, rare species do not contribute meaningfully to compositional examination; we therefore excluded taxa and morphospecies from analyses when they appeared at fewer than four sites. We also conducted post-hoc tests using ManyGLM to determine which taxon or species responded most strongly to our predictors. We then ran pairwise comparisons in ManyGLM to determine which fire severities differed from each other. We show unadjusted P-values for post hoc tests because there were a large number of comparisons and we considered that adjusted tests would have been overly conservative (increased Type II error). However, this approach does increase the likelihood of Type I error (Garcia, 2004). We visualised the effects of

3. Results We collected 23 taxa and 1766 individuals overall. Six taxa and 222 individuals were associated with logs and 23 taxa and 1544 individuals were collected from litter bags. We collected 21 beetle (Coleoptera) morphospecies and 258 individuals. 3.1. Taxon richness Taxon and beetle species richness were significantly lower at crown burnt than unburnt sites, (R2 = 0.46, F(2,18) = 9.528, P = 0.001 and R2 = 0.2083, F(2,17) = 22.3, P = 0.043, respectively) (Fig. 3a and b), confirming that sites that experience high severity fires support lower richness of litter-dwelling macroinvertebrates three years after fire. Ground burnt sites supported intermediate richness. 3.2. Species traits: trophic groups, body size and wing presence Both predator and non-predator abundance declined with increasing fire severity, as predicted (Table 1, Fig. 3c). Although the proportion of predators increased with increasing fire severity, this relationship was not significant (Table 1). As expected, non-predator size was greatest at crown burnt sites and declined with increasing levels of moisture in the best model (Table 1, Fig. 3d). Predator body size tended to be greater with increasing fire severity (marginally non-significant) and moss cover and declined with increasing soil disturbance and moisture (marginally non-significant) in the best model (Table 1; Fig. 3). Neither minimum (F(2,18) = 2.29, p = 0.130), maximum (F(2,18) = 0.35, p = 0.709), nor median (F(2,18) = 1.79, p = 0.196) 282

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a)

a

b) a

ab

ab

b

b

d)

c)

b

c a

a a

a a

d e

a

b

b

Fig. 3. Mean ± SE richness of litter-dwelling macroinvertebrates per site by (a) Taxon richness, (b) Morphospecies richness, and mean ± SE of: (c) predator (light grey) and non-predator abundance (dark grey); (d) predator (light grey) and non-predator (dark grey) body length under three different fire severities. Columns with different letters above were significantly different in post-hoc tests.

body size differed among fire severity classes. Predictions that the percentage of taxa that were winged (i.e., with good dispersal ability) would increase with fire severity were not supported for predators or non-predators, although the trend was consistent with predictions for winged non-predator taxa (Table 2, Fig. 4a, c and d). Our hypothesis that there would be a higher percentage of predators at crown burnt than unburnt sites was also not supported, although the trend was consistent with predictions (Table 2, Fig. 4b).

high severity sites differed from those at low severity and control sites (unburnt vs crown burnt: Dev = 78.23, P = 0.004; and ground burnt vs crown burnt: Dev = 46.77, P = 0.033), while unburnt and ground burnt sites were not different (Dev = 44.02, P = 0.084) (Table 3, Fig. 5a). However, we did not detect any differences for invertebrates collected from logs (Table 1), possibly because fewer individuals were collected from this substrate. ManyGLM post-hoc tests showed that seven taxa responded negatively to increasing fire severity: non-biting midges (Diptera: Chironomidae, 44% of individuals); crane flies (Diptera: Tipulidae) and bibionid flies (Diptera: Bibionidae); flat-backed millipedes (Polydesmida: Dalodesmidae); native rolling woodlice (Isopoda: Armadillidae); bugs (Hemiptera); and earthworms (Annelida) (Table 3). ManyGLM post-hoc tests showed that six of 23 taxa in

3.3. Composition Fire severity significantly affected the composition of invertebrates collected with litterbags, consistent with predictions. Composition at

Table 1 OLS regression testing the effect of fire severity and seven microhabitat variables on: (a) total abundance; (b) predator abundance percentage; (c) Predator size; and (d) Non-predator size. GLM regression testing was used for percentage response variables. For direction (D) a (−) sign indicates a negative effect and (+) sign indicates a positive effect; *p < 0.05, **p < 0.01, ***p < 0.001. Predator abundance percentage for the whole model produced a quasivariance value (or an approximation of real value) to correct for overdispersion and therefore an AIC model-stepwise regression for the best fit model could not be made. Model

Total abundance

Predator size

Non-predator size

Whole

Best fit

Whole

Whole

Best fit

Whole

Best fit

d.f. = 9,11

d.f. = 7,13

d.f. = 9,11

d.f. = 9,11

d.f. = 5,15

d.f. = 9,11

d.f. = 4,16

F

F

F

F Fire Severity Foliage Cover Bare Soil Moss Cover Litter Depth Soil Disturbance Moisture Distance to Log

Predator abundance (%)

24.94 0.00 4.41 0.48 4.03 0.39 0.03 3.89

D

F ***

(−) (−) (−). (−) (−). (+) (+) (+).

D

F ***

29.65

(−)

5.25

(−)*

4.45

4.11

(−).

(−).

3.02 2.41 0.01 0.28 0.30 6.04 2.33 3.51

D (+). (+) (−) (+) (−) (+)* (+) (−).

3.05 2.99 1.02 5.24 1.19 6.10 1.66 0.77

283

D (+). (+) (+) (+)* (+) (−)* (−) (+)

D

3.39

(+).

8.41

(+)*

6.30 3.58

(−)* (−).

10.88 0.00 5.57 0.02 0.07 0.97 9.29 0.99

D ***

(+) (+) (+)* (−) (+) (+) (−)* (+)

F

D

14.47

(+)***

5.52

(+)*

12.40

(−)**

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Table 2 GLM regression testing the effect of fire severity and seven microhabitat variables on the percentage of: a) taxa with wings; b) predator taxa; c) winged predator taxa; and d) winged non-predator taxa. For direction (D) a (−) sign indicates a negative effect and (+) sign indicates a positive effect; *p < 0.05, **p < 0.01, *** p < 0.001. Model

Taxa with wings

Fire Severity Foliage Cover Bare Soil Moss Cover Litter Depth Soil Disturbance Moisture Distance to Log

Predator taxa

Winged predator taxa

Winged non-predator taxa

Whole

Best fit

Whole

Best fit

Whole

Best fit

Whole

Best fit

d.f. = 9,11

d.f. = 2,18

d.f. = 9,11

d.f. = 2,18

d.f. = 9,11

d.f. = 3,17

d.f. = 9,11

d.f. = 2,18

F

D

F

D

F

D

F

D

F

D

F

D

F

D

F

D

0.53 0.05 1.42 0.50 0.02 0.10 0.02 0.01

(+) (−) (−) (−) (+) (−) (−) (+)

0.53

(+)

0.43 0.04 0.00 0.35 0.04 0.03 0.05 0.36

(+) (−) (+) (−) (+) (−) (−) (+)

0.43

(+)

0.58 0.06 0.15 2.02 0.08 0.65 0.72 1.24

(−) (−) (+) (−) (+) (−) (−) (+)

0.58

(−)

(+)

(−)

(+) (−) (−) (−) (−) (−) (−) (+)

0.73

1.11

0.73 0.02 1.53 0.00 0.00 0.00 0.22 0.52

b)

a)

a a

a a

a

a

c)

d)

a

a a a a a

Fig. 4. Mean ± SE percentage of: (a) winged taxa, (b) predator taxa, (c) winged predator taxa and (d) winged non-predator taxa under different fire severities. Columns with different letters above were significantly different in post-hoc tests. 284

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Table 3 ManyGLM regression testing the effect of fire severity and seven microhabitat variables on the composition of litter-dwelling macroinvertebrate taxa collected using litterbags. Summary is the overall effect of variable on composition. Decreasers and Increasers refers to negative and positive responses by taxa in post-hoc tests, respectively. Asterisks next to taxon names indicate significant effects in post-hoc tests. *p < 0.05, **p < 0.01, ***p < 0.001. Source

Taxon (litter) Deviance **

Fire Severity

110

Foliage Cover Bare Soil

13.3 47.1*

Moss Cover Litter Depth Soil Disturbance Moisture

31.0 23.3 58.1 90.1**

Log distance

49.3

Responders **

**

*

*

Decreasers: Dalodesmidae , Armadillidae , Bibionidae , Chironomidae , Tipulidae*, Hemiptera*, Annelida* Decreasers: Chironomidae*, Brachycera* Increasers: Talitridae**, Styloniscidae**, Curculionidae* Decreasers: Opiliones** Increasers: Opiliones**, Curculionidae*, Hemiptera* Decreasers: Lepidoptera**, Formicidae*; Increasers: Dalodesmidae**, Sciaridae*, Opiliones*

Taxon (logs)

Coleoptera

Deviance

Deviance

Responders

13.0

28.9

5.3 1.1

5.6 2.9

10.0 2.6 10.5 26.7**

20.4 23.5 15.0 13.2

1.3

Increasers: Dalodesmidae** Philosciidae** Talitridae*

8.4

Fig. 5. Nonmetric multidimensional scaling plots of litter-dwelling macroinvertebrate assemblage composition at: (a) taxon; and (b) species level (Coleoptera only), at 21 sites for three different fire regimes (Unburnt, open; Ground Burnt, grey; Crown Burnt, black).

Woodward et al., 2005; Williams et al., 2010), increased with fire severity. We discuss these findings in the context of the temporal stage at which mechanisms that regulate species reassembly are likely to operate: during the fire or in the short- or longer-term post-fire environment and consider dispersal, physiological and resource-based mechanisms. Severe fires had lasting effects on macroinvertebrates: three years after fire, we detected clear differences in the richness and abundance of coarsely and finely defined taxa among fire severity classes. We found clear evidence of low abundance following severe fires among dalodesmid millipedes; armadillid (but not other) woodlice; detritivorous flies (tipulids, chironomids, bibionids); Hemiptera and Annelida. That there were effects on armadillid, but not other woodlice, was surprising as armadillids from this study area have a higher CTmax (but not higher desiccation tolerance) than other terrestrial isopods (Grubb et al., in review). However, this pattern might be explained by differences in dispersal ability. Effects on other taxa were not surprising: for example, dipterans may decline in response to high frequency fires (Brennan et al., 2009), while Polydesmid millipedes, including the Dalodesmidae, commonly exhibit fine-scale parapatry that suggests movement that would allow recolonisation is limited (e.g., Mesibov, 2011). The post-fire environment differed among fire severity classes (Buckingham et al., 2015): vertebrate-driven soil disturbance at the study sites declined with increasing fire severity, while moss cover increased. Extreme abiotic environments are associated with macroinvertebrate diversity declines (Chase et al., 2012). Increased bare ground and reduced moisture were associated with declines in flies, probably because their larvae require moist, sheltered conditions. In contrast, taxa such as ants and moths did better in drier sites, reflecting their superior desiccation tolerance. Although the loss of habitat complexity can also inhibit recolonization or persistence following fire

litterbags were significantly more abundant at unburnt sites than crown burnt sites. Taxa that declined in response to high severity fires were predominantly non-predators: Chironomidae; Bibionidae; Armadillidae; Dalodesmidae, Hemiptera; and Annelida. Terrestrial crustaceans, i.e., landhoppers (Amphipoda:Talitridae) and most native woodlice (Isopoda:Styloniscidae and Philosciidae), were unaffected by fire. Beetle species composition in litterbags did not differ significantly among fire severities (Table 3, Fig. 5b). There was no indication that increasing fire severity was associated with an increase in abundance for any taxon or beetle species. Some taxa responded strongly to microhabitat variables. Leaf-consuming moths (Lepidoptera), the second-most abundant group (27% of total assemblage) did not respond to fire severity, but decreased with increasing moisture, while dalodesmid millipedes responded negatively to high fire severity and positively to higher moisture conditions (Table 3). High abundances of talitrid and styloniscid crustaceans and low abundances of chironomid and brachyceran fly larvae were associated with bare soil. 4. Discussion The frequency of high severity fires is expected to increase with global warming, so it is critical that we understand the impact of high severity fires on biodiversity. We asked if assemblages of macroinvertebrate litter fauna change in response to increasing fire severity and whether the effects of fire severity on species depend on species traits. We found clear declines in beetle species and overall taxon richness and abundance with increasing fire severity. We also found changes in taxon, but not beetle species composition. We found only weak (non-significant) evidence that these changes might be driven by dispersal (wing presence) or trophic traits of species. However, body size, a key trait with many known functions (Ritchie and Olff, 1999; 285

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recolonisation following fire. Further testing of the links between wing traits (Buckingham, 2016), desiccation avoidance behaviour and tolerance may help determine the mechanisms driving taxon loss after fires and provide a stronger framework for predicting species responses.

(Smucker et al., 2005), the link between fire severity and litter cover at the study sites was weak (Buckingham et al., 2015). We suggest that the negative relationship between abundance and fire severity may reflect both the current, relatively fine-scale differences in microhabitats, and the simplified and drier microclimates immediately following severe fires. Persisting differences in microhabitat may be compounded by the failure of species that were unable to persist through the fire to recolonise high severity burn sites within three years. Amongst the traits examined, body size is the most likely to affect in situ survival as increasing body size is correlated with greater desiccation tolerance (Edney, 1977; Renault and Coray, 2004; Dias et al., 2013), improved dispersal ability (With, 1994; Farji-Brener et al., 2004), and resistance to starvation (Cushman et al., 1993; Kaspari and Vargo, 1995), all of which enhance the probability of survival during fire and shortly after, but large body size might also limit access to temporary refuges. Average body size of non-predators was greater following high severity fires, as predicted, because of the reduction in smaller dipterans, such as chironomids. However, it is unclear whether this is because these smaller species were unable to survive the fire, failed to persist in the desiccating and resource-poor post-fire environment or were unable to disperse to burnt sites as habitat returned. In contrast, predator body size was unaffected by fire severity, perhaps because many predators are active hunters and therefore likely to be more mobile and desiccation-tolerant than non-predators. Immediate post-fire sampling would help to disentangle the mechanisms driving these patterns. Food resources are critical to the persistence of species. We expected predator species to make up a greater proportion of the litter macroinvertebrate community at burnt sites in the early stages of succession because hunting efficiency is greater in open habitats (Crawford et al., 1995; Polis and Strong, 1996), such as those formed by fire. Further, resources for other trophic groups, particularly detritivores, are lower in litter-poor post-fire habitats (York 1999). Almost all taxa that declined with increasing fire severity were detritivores, including dalodesmid millipedes, armadillid isopods, bibionid, chironomid and tipulid flies and annelid worms. Although litter was similar across fire severity classes three years after fire, the proportion of predators tended to be greater in severely burnt sites. This might reflect a legacy of earlier litter-poor post-fire habitats. Species that are unable to survive the fire or the early stages of the post-fire environment must disperse if they are to recolonise and survive harsh climatic conditions. Although trends for non-predators were in the expected direction, our prediction that there would be a greater proportion of species with wings (good dispersers) in sites that had experienced higher fire severity was not supported. Larger body size may also enhance dispersal ability for both winged (den Boer, 1990; Gathmann et al., 1994; Steffan-Dewenter and Tscharntke, 1997; Jennings and Tallamy, 2006; Jenkins et al., 2007; Soininen et al., 2007; Sekar, 2012; Stevens et al., 2014) and flightless species (With, 1994), but larger body size is associated with winglessness (e.g., beetles, Gibb et al., 2017). Rather than considering traits in isolation, it may therefore be important to consider trait complexes when assessing recolonisation success. Flightless taxa such as terrestrial amphipods, crustaceans and millipedes have limited dispersal capacity (Kotze and Lawes, 2008; Magrini et al., 2011; Mesibov, 2011), but some taxa may persist in situ and have high reproductive capacity so recover rapidly following fire. In contrast, winged non-predatory flies (tipulids, chironomids, bibionids), which did poorly following high severity fires, are characteristically limited by a suite of characteristics that reduce their ability to recover following fire: they are poor fliers, have low desiccation tolerance and show a limited array of desiccation avoidance behaviours (Pritchard, 1983; Ellington, 1984; Delletre, 1994; Frouz and Kindlmann, 2001; Frouz and Šimek, 2009; Nation, 2015). Another winged taxon, the moths, builds shelters (Dugdale, 1996; Fukui, 2001) and enters diapause during periods of stress (Bauce and Han, 2007) and this combination of traits may allow persistence and rapid

5. Conclusions Fire frequency and severity are expected to increase in the future (Johnson et al., 2001; Macias Fauria and Johnson, 2008; Cruz et al., 2012). High fire severity was associated with a marked reduction in abundance and taxon richness, a change in assemblage composition and an increase in the body size of litter-dwelling macroinvertebrates three years after fire. We therefore predicted that climate-change associated changes in fire severity will result in declines in species richness, with smaller species negatively affected. This contrasts with predictions that shrinking body size will always be a consequence of global change (Easterling et al., 2000; Gardner et al., 2011; Sheridan and Bickford, 2011), but is partially in agreement with findings that habitat disturbances affect species at the extremes of size (Gibb et al., 2018). While this study shows that fires of higher severity result in litter assemblages with fewer species and individuals, our previous work in this system indicates that litter decomposition changes little, suggesting high functional redundancy (Buckingham et al., 2015). We suggest that a more mechanistic understanding of species responses to high severity fires might be obtained by further investigating physiological tolerance and by considering complexes of traits to better represent the varieties of strategies that allow persistence following high severity fires. Studies should ideally commence prior to fires and extend over longer periods of time since fire and during periods of drought that are likely to intensify changed microclimatic conditions. Understanding how and when traits allowing persistence and recolonisation interact will provide greater insights into the challenges that species face in the post-fire environment. Acknowledgements We thank Natasha Robinson, and Steve Leonard with assistance in mapping and site selection for this research. We are grateful to Don Driscoll and Joakim Hjältén for comments that helped improve the manuscript. Thanks to Angie Haslem and Simon Watson for statistical advice and use of software and Ion Maher and Tony Fitzgerald from Kinglake National Park, ParksVic who facilitated access to sites. We are grateful to the Department of Sustainability and Environment (funding to HG and NM) and La Trobe University (La Trobe University postgraduate research scholarship to SB and the School of Life Sciences 2016 Postgraduate Publication Grant to HG & SB) for funding this project. Appendix A. Supplementary material Supplementary data to this article can be found online at https:// doi.org/10.1016/j.foreco.2018.12.030. References Ashton, D.H., 1975. Studies of litter in Eucalyptus regnans Forests. Aust. J. Bot. 23, 413–433. Attiwill, P.M., 1979. Nutrient cycling in a Eucalyptus obliqua (L'Hrit.) forest. III growth, biomass, and net primary production. Aust. J. Bot. 27, 439–458. Banks, S.C., Dujardin, M., McBurney, L., Blair, D., Barker, M., Lindenmayer, D.B., 2011. Starting points for small mammal population recovery after wildfire: recolonisation or residual populations? Oikos 120, 26–37. Bassett, M., Chia, E.K., Leonard, S.W.J., Nimmo, D.G., Holland, G.J., Ritchie, E.G., Clarke, M.F., Bennett, A.F., 2015. The effects of topographic variation and the fire regime on coarse woody debris: insights from a large wildfire. For. Ecol. Manage. 340, 126–134. Bauce, É., Han, E., 2007. Desiccation resistance in pre-diapause, diapause and post-diapause larvae of Choristoneura fumiferana (Lepidoptera: Tortricidae). Bull. Entomol. Res. 91. Booth, R.G., Cox, M.L., Madge, R.B., 1990. Coleoptera. CAB International, International

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