It is generally expected that landscape changes, such as habitat loss and fragmentation, should negatively affect functional diversity metrics, which in turn impact ecosystem functioning. In this review, we search for studies conducted in the tropics and published in the last 10 years to understand how different aspects of landscape change affect functional diversity metrics and how the latter are associated to ecosystem functioning. In total, we found 24 papers that assessed the effects of landscape metrics on functional diversity, evenness, divergence and composition, and although there was a general trend for functional diversity metrics to improve with habitat cover, we found a wide range of responses. Most surprisingly, however, we only found five studies from the tropics assessing the extent to which functional diversity metrics were correlated to measures of ecosystem functioning, and in general, very weak support was found. In conclusion, our results show that it is crucial to first investigate the level to which functional diversity metrics truly represent or may lead to changes in ecosystem functioning, and this is particularly important for animal communities in the tropics. Without such confirmation, there is little reason to pursue further work to reach a consensus regarding how landscape modification affects functional diversity metrics. . . . . Keywords Ecosystem functioning Ecosystem processes Functional diversity Functional traits Tropics Introduction prism of functional diversity metrics, as a step away from the simplicity of biodiversity and ecosystem functioning It is unambiguous that habitat loss and fragmentation are lead- (BEF) approaches, towards the representation of functional ing drivers of the global decline in terrestrial biodiversity ; traits within a community . Such an approach, however, however, their effects on ecosystem functioning are still de- relies on the assumption that functional diversity metrics and batable [2 , 3]. The impact of landscape alteration on ecosys- ecosystem processes are strongly associated. Here we review tem functioning has been commonly studied through the the literature to assess how habitat changes affect functional diversity metrics, and we search for evidence of the extent to which functional trait diversity impacts ecosystem processes. Jack H. Hatfield and Michelle L. K. Harrisson would like to be recognised Functional diversity metrics are calculated by associating as first authors. species-by-site matrices, such as presence-absence or abun- This article is part of the Topical Collection on Effects of Landscape dance of species, to the species’ functional traits; i.e. morpho- Structure on Conservation of Species and Biodiversity logical or behavioural traits that are related to the role the Electronic supplementary material The online version of this article species may perform in the ecosystem [5� ]. Historically, the (https://doi.org/10.1007/s40823-018-0032-x) contains supplementary first metrics to be used in ecological studies were the richness material, which is available to authorized users. of functional groups. However, since the seminal work of Petchey and Gaston , functional diversity went on to be * Cristina Banks-Leite measured with an approach similar to that employed for quan- email@example.com tifying phylogenetic relatedness, and a wealth of new metrics to assess distinct components of diversity have been produced, Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot SL5 7PY, UK such as functional evenness and divergence [7� ]. Metrics based on functional traits are direct analogues of community Department of Ecology, Biosciences Institute, Universidade de of São Paulo, São Paulo, SP 05508-090, Brazil metrics and, similarly to species diversity, functional diversity �� 36 Curr Landscape Ecol Rep (2018) 3:35–42 is the most commonly employed and supposedly the most powerful measure of variation in functional traits [5� , 8]. The popularity of functional diversity metrics can be seen in the landscape ecology literature, where a number of studies have employed these measures to better understand how land- scape change affects communities and ecosystems [9–11]. Observed changes to functional diversity metrics are interpreted as direct evidence that rates of ecosystem processes are also affected. Indeed, for temperate plants, there is enough evidence to suggest that functional diversity measures are highly corre- lated to rates of ecosystem processes (Fig. 1a) [13, 14]. However, ecosystem processes regulated by animals are often performed by more than one taxon [2�� ]. For instance, pest predation may be performed by birds and spiders, and a reduc- tion in the functional diversity of insectivorous birds may not Fig. 1 Schematic representation of how landscape change may influence affect pest regulation if the functional diversity of spiders in- ecosystem functioning (EF) through changes in functional trait metrics. creases (Fig. 1b). It is thus still unclear how changes in animal The current widespread expectation is that landscape changes negatively affect functional trait metrics, and in turn, the outcome on EF will also be abundances, and their associated traits, affect ecosystem func- negative (a). However, landscape changes may negatively affect some tions . Furthermore, such overlap in functions performed by taxa while positively affect others, and the net result of these changes onto different animal taxa is likely to be more prominent in tropical EF is neutral (b). See Ewers et al. [2 ] for an example of b. Furthermore, ecosystems , suggesting that patterns observed for the tem- landscape changes may not affect functional trait metrics, such as functional diversity, but affect other community metrics such as species perate zones may not be applicable to the tropics. In the same turnover, or species specialisation. The net result of these changes will be way that hundreds of studies have assessed the links between a negative impact of ecosystem function. See de Coster et al. [12�� ]and biodiversity and ecosystem functions across a range of ecosys- text for an example of c tem (see  for a review), it is crucial that we fully understand whether functional diversity metrics can be indeed used as a “structural connectivity”), 3. “functional diversity” AND trop- proxy for ecosystem functioning. ic* AND “habitat loss” AND fragment*. Studies were restrict- Here, we reviewed the last 10 years of ecological literature to ed to those that were (1) conducted in the tropics and (2) determine (1) how functional diversity metrics are affected by examined a gradient of landscape fragmentation and (3) made land cover and measures of landscape configuration and (2) a quantitative assessment of functional diversity. how functional diversity metrics are related to rates of ecosys- Similarly, we conducted two searches to find published tem processes and ecosystem functions. Our search was restrict- articles about functional diversity metrics and ecosystem func- ed to the tropics as they hold a large proportion of worldwide tions using the following set of terms: 1. “functional diversity” biodiversity , are at high risk from land use change [19, 20] AND tropic* AND (“ecosystem service” OR “ecosystem pro- and perform globally important ecosystem functions [21, 22]. cess” OR “ecosystem function”), 2. “functional diversity” We also focused only on terrestrial and riverine systems as AND tropic* AND (“pollination” OR “insectivor*” OR “seed landscape configuration is quantified in a different way for large dispersal” OR “decomposition” OR “carbon stocks” OR “ni- aquatic systems due to its three-dimensional structure . trogen”). These specific terms were chosen to reflect the pri- mary functions performed by vertebrates, invertebrates and plants within tropical ecosystems. Methods We searched the Web of Knowledge and Google Scholar for articles published between 2006 and 2016. Searches were Results conducted in December 2016 and January 2017. Google Scholar searches were continued until two pages in a row Functional Diversity Metrics and Landscape (20 records) contained no relevant results. Configuration Published articles on the topic of landscape configuration and functional diversity metrics were selected based on the In total, we found 24 published articles that investigate the following search terms: 1. “functional diversity” AND tropic* effects of land cover and landscape configuration on different AND (“patch size” OR “fragment size”), 2. “functional diver- functional diversity metrics (Table 1;Table S1). A range of taxa sity” AND tropic* AND (“habitat connectivity” OR “land- were studied incorporating plants, invertebrates and vertebrates scape connectivity” OR “functional connectivity” OR but the number of habitat types was limited, with most studies �� Curr Landscape Ecol Rep (2018) 3:35–42 37 Table 1 Table summarising the results of referenced studies comparing functional diversity metrics to landscape metrics Functional metric Fragmented vs. reference Edge effects Patch size Habitat percentage Connectivity Diversity/richness + [24–27] + [24, 30] + [9, 28, 32, 33] + [35, 36] +  0 [28, 29] 0 [11, 31] 0 [11, 34] 0[12 ] ~  −  Evenness +  +  0  +  0  0  ~  0 [36, 37] −  − [12�� ] Divergence/dispersion + [25, 38] +  0  0  −  0  0[11, 31] − [11, 39] − [37, 40, 41] Integrity/composition ~  + [12�� ] Similarity (functional β-diversity) −  −  The directionality of relationship is given in bold. A positive correlation indicates higher functional diversity in increasingly intact habitat. Categorisation of functional metrics was largely based on Mouchet et al. [7� ] + positive correlation, 0 no clear correlation detected, − negative correlation, ~ non-linear or unstated relationship focusing on forest systems. Geographically, the majority of mammal communities, Ahumada et al. also found studies concentrated on the Brazilian Atlantic and Amazon for- that functional dispersion was higher in continuous forest ests, with nearly all studies focusing on Central and South when compared to fragments. However, this pattern did America. Landscape configuration was assessed in a number not hold for other taxa—no differences in functional of ways. The simplest method was the comparison of richness, evenness or dispersion were observed when fragmented or edge habitat to its equivalent continuous or pris- comparing dung beetle communities between fragments tine reference site. Other studies looked at individual landscape and continuous forest  or when assessing the varia- metrics such as patch size, patch shape, connectivity and per- tion in functional richness of Atlantic Forest avian com- centage of focal habitat. We summarise the different approaches munities between mature forest and regenerating frag- used in five main categories: (1) comparisons between contin- ments . While the majority of studies focused on uous and fragmented habitat, (2) edge effects, (3) patch size, (4) functional measures analogous to α-diversity, Sfair percentage habitat cover and (5) connectivity (Table 1). et al.  examined functional β-diversity in plants. Overall habitat loss and fragmentation reduced functional They found it to be higher in fragments than old growth diversity, but there were some exceptions and the nature of the forest and highest at fragment edges . This indicates change showed considerable variation. Many studies also that functional diversity exhibits greater heterogeneity in compared the responses of species richness to habitat loss fragments (especially edges) as opposed to continuous and fragmentation, and these responses were mostly in agree- forest, but patterns were less clear when considering only ment with those observed by functional response metrics species occurrence as opposed to abundance . (Table S2). Because of the large variation in taxa, biome, (2) Edge effects: The altered abiotic conditions in edge hab- functional and landscape metrics used, the evidence (or lack itats  can have substantial effects upon community thereof) to support the existence of a relationship between and ecosystem processes [45, 46], and edge effects may functional metrics and landscape metrics was usually obtained even be the cause of many observed area effects . from one or few studies. Despite such pervasive impacts, we could not find a con- sensus regarding their effects on functional diversity (1) Fragments vs. continuous forest: The majority of studies metrics (Table 1). The functional evenness of tree com- detected an increase in functional diversity in continuous munities and diversity of their pollination syndromes habitatincomparisonwithfragmented[24–27, 38] were reported to be higher in fragment interiors than (Table 1). Pollination syndromes were more diverse in edges [11, 27]; however, no changes in richness or diver- continuous forest than in fragments [24, 27], and tree gence were found . No differences were found for seedling assemblages also differed in functional compo- forest herpetofauna in forest-oil palm systems when sition between small forest fragments and sites in mature functional richness, evenness and divergence were con- forest . Even when compared to naturally sidered . Overall this suggests that the effect of edges fragmented forest, continuous forest was found to have on functional diversity is less clear than the overall ef- higher functional richness, evenness and divergence in fects of fragmentation. Assessing the impacts of patch plant communities . Continuous forests were found shape is another approach to understanding the impor- to harbour higher functional richness of mammals than tance of edge effects. This is because as patch shape riparian fragments . In their pan-tropical study of becomes increasingly irregular, the amount of edge �� 38 Curr Landscape Ecol Rep (2018) 3:35–42 habitat relative to area increases. Patch shape was con- independent measure of ecosystem processes in tropical sys- sidered in only two studies, both of which found that tems. Only two taxa were assessed (birds and plants) and only more compact patches supported communities with a four functions were measured (seed dispersal, pest control, more diverse array of functions, with higher functional aboveground biomass and carbon storage). The overall result diversity  and divergence . is that although functional diversity metrics are somehow cor- (3) Patch size: A positive relationship between patch size and related with ecosystem processes, functional diversity per se is functional richness was found for copro-necrophagous not a good predictor of ecosystem functioning. However, with beetles , mammals , trees  and vertebrates only five studies, we are unable to draw any firm conclusions . Nonetheless, these results did not hold for all plant or provide any meaningful insight. communities orbirds, in which functional rich- Bird functional diversity metrics were shown to be weakly ness was found to vary independently of patch size. correlated with the provisioning of pest control, but may pro- Similarly, no effects of patch size were found on function- vide a better proxy for seed dispersal. A meta-analysis of nine al evenness or divergence of beetle assemblages . In avian exclusion studies in tropical coffee and cacao agro- contrast, a negative correlation was reported for patch size forests compared the predictive power of species richness and functional divergence in phyllostomid bats and and functional diversity metrics in determining arthropod pre- trees . More complex patterns have been observed, dation . Functional richness exhibited a higher degree of such as a non-linear relationship with patch size . correlation with arthropod predation when the metric included (4) Habitat amount: Mammal functional richness was posi- multiple traits, highlighting the importance of trait selection tively correlated with forest cover , as was avian func- when using measures of functional diversity. However, func- tional richness in agricultural and arable landscapes . tional group richness was a better predictor of ecosystem func- For bird species in forest fragments, no link between func- tioning than functional diversity metrics, and most important- tional richness and forest cover was found and evenness ly, species richness provided the strongest predictive power of decreased with increasing forest cover; however, function- all the metrics. Another study investigated how functional al integrity (similarity to control sites) increased with for- diversity related to frugivorous birds’ activity and seed dis- est cover . This suggests a change in species ’ func- persal in different habitats . The proportion of interactions tional traits, producing a new functional space that is no between frugivorous birds and fruit was two times greater in less diverse. The functional richness and dispersion of edge habitat than within the forest interior. Functional richness riverine fish communities decreased with increasing forest was greater at the forest edge and correlated with the higher cover, but evenness remained unaffected and the findings number of fruit–bird interactions. Variation in functional rich- differed dependent on local habitat type . In contrast, ness between the two habitat types was also associated with some research indicates that the nearest taxon index is changes in plant species diversity. However, this study did not negatively associated with forest cover, suggesting forest- include any other measure of seed dispersal, such as seed rain ed streams have more functionally complementary fish or seed viability; thus, it remains to be confirmed whether communities . For trees, a negative correlation was greater functional richness of birds does indeed lead to in- found between functional divergence and natural vegeta- creases in seed dispersal. tion cover . These conflicting results may suggest a In plants, functional dominance has been shown to be a shift between two communities, both of which are func- better proxy for carbon storage than functional richness. The tionally diverse yet distinct. The effect of habitat cover is role of functional diversity metrics as a determinant of carbon also highly dependent on scale  and the results may be storage was investigated in natural tropical forest in Panama affected heavily by the gradient examined. . Functional dominance accounted for most of the varia- (5) Connectivity: Compared with previous landscape met- tion in carbon storage in natural forest sites. A broader study, rics, few studies explicitly examined connectivity. encompassing natural tropical forest sites across Africa, Asia Mammal functional richness was found to correlate pos- and the Americas, reported similar findings . The carbon itively with connectivity , whereas work on bats in- storage capacity of 11 tropical forests was most strongly cor- dicates that their functional divergence decreased as related with increased functional dominance and taxonomic proximity to other patches increased . diversity, but not with functional diversity. However, the study results suggest that the suitability of plant functional diversity indices to predict carbon storage capacity may vary depending Functional Diversity Metrics and Ecosystem on forest type . In a similar study of three neo-tropical Functioning forests, aboveground biomass was found to correlate positive- ly with key individual plant functional traits, most significant- We found only five studies published in the last 10 years that ly with wood specific gravity and maximum adult height. In contrast, there was no relationship between aboveground quantified functional diversity metrics alongside an �� Curr Landscape Ecol Rep (2018) 3:35–42 39 biomass and functional variety as measured by functional these results may have been generated. Fragmented land- richness, evenness, dispersion and divergence . scapes may provide a wider range of habitat types and hence niches—therefore, they may have less niche homogenisation  and contain a community with a more diverse array of Discussion traits . Heterogeneous landscapes may support a wider range of species, hence occupying a greater area in trait space. It has been generally expected that habitat loss and fragmen- Nonetheless, an increase in functional divergence in tation have detrimental effects on functional diversity metrics, fragmented habitats does not necessarily mean that the func- which in turn will negatively affect ecosystem functioning tions are similar to those performed in pristine habitats and (Fig. 1a). Based on current empirical evidence, our results does not mean that ecosystem functioning will be positively indicate that only some of these expectations are warranted impacted. for tropical landscapes. Although the majority of studies re- We were surprised, however, to find such weak evidence ported higher functional diversity or richness in more pristine supporting the view that functional metrics are correlated to habitats (Table 1), there was little consensus among studies ecosystem functioning or ecosystem dynamics. Not only did that investigated additional functional diversity and landscape we find just five studies, but they failed to show overwhelm- metrics. There is an even greater lack of clarity regarding the ing support for the use of functional diversity metrics as a interplay between functional metrics and ecosystem functions, proxy of ecosystem functioning. Even species richness, which as only five studies with contradictory results were found. is a notoriously poor community metric [60–62], was found to A number of potential issues could be underlying such be better than functional richness in predicting the perfor- unmet expectations. It is possible that functional metric pat- mance of some ecosystem functions. Further research is vital terns are more complex than originally thought due to the in establishing the link between functional diversity metrics idiosyncrasies of individual taxa—bats, for example, often and ecosystem functioning, and there are at least two reasons show conflicting patterns when compared to other taxa. why this link may not be strong. Firstly, functional metrics are There may also be geographic differences, with abiotic and usually only measured from the perspective of one taxon. biotic factors unique to a particular site or region, exerting a Such a modular view of ecosystem dynamics likely fails to strong influence on the nature of functional changes. The role assess distinct groups that often perform similar functions, and of temporal and site-specific differences is starting to be which may show contrasting responses to habitat change recognised when comparing sensitivity (or response) traits to (Fig. 1b). A prime example of this occurs in Borneo, where landscape change [54–56], and the situation may be similar ecosystem functions are maintained across a gradient of hab- for functional traits, making generalisation difficult. itat disturbance, despite marked declines in key species [2�� ]. Trait choice is of extreme importance for analyses using In human-modified habitat, invertebrate groups, such as ter- functional metrics as the inclusion of traits unrepresentative mites, ants, beetles and earthworms, decrease in abundance of function, or the exclusion of traits that are functionally [2�� ]. However, decomposition, seed consumption and inver- important, can both influence the validity of the results [6, tebrate predation are still performed at the same rates, as ver- 57]. Notwithstanding, studies on similar taxonomic groups tebrates take up the lead role in those functional groups [2�� ]. most commonly differ in their trait selection [35, 38]. On the Had these authors only focused on functional diversity of other hand, many studies still focus on species richness of invertebrates, they would have reported a strong decrease in functional groups. This is a coarse measure of functional di- ecosystem functioning. Secondly, there may be situations versity, which is impervious to within-group variation, and where functional richness does not vary, but ecosystem func- has been found to explain less variation in ecosystem func- tioning is impacted (Fig. 1c). For instance, functional richness tioning than more complex metrics . of birds in the Atlantic Forest of Brazil does not vary mean- Finally, the effects of habitat fragmentation are highly con- ingfully, but dietary specialisation is significantly reduced by text dependent . The intervening matrix and amount of habitat loss [12�� ]. Specialist insectivores are believed to have habitat cover in the region can modify how species respond a stronger impact on insect populations than generalist insec- to patch size and isolation, making it difficult to obtain clear tivores ; thus, potentially, the strength of arthropod control patterns even for simpler metrics such as species abundance is diminished in more deforested sites despite absence of var- and species richness [59, 60]. And in the same way that habitat iation in functional richness. fragmentation can improve some community metrics (such as beta-diversity), it may also have positive consequences for some functional metrics. For example, Magnago et al.  Conclusions found functional divergence to decrease with increasing patch size, whereas the majority of authors found an increase with Due to the small sample of published articles yielded by the patch size [9, 28, 32, 33]. There are a number of reasons why literature search, it is impossible to draw any firm conclusions 40 Curr Landscape Ecol Rep (2018) 3:35–42 article demonstrates the importance of considering multiple about the performance and suitability of functional diversity taxa when examining functional diversity. metrics in predicting ecosystem function in tropical land- 3. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, scapes, and this is particularly important for animal taxa. et al. Effects of biodiversity on ecosystem functioning: a consensus Although a larger pool of studies have been conducted on of current knowledge. Ecol Monogr. 2005;75:3–35. 4. Reiss J, Bridle JR, Montoya JM, Woodward G. Emerging horizons the effects of landscape change on functional metrics, the pic- in biodiversity and ecosystem functioning research. Trends Ecol ture remains unclear due to the abundance of contrasting re- Evol. 2009;24:505–14. sults. Although species diversity and functional diversity are 5.� Petchey OL, Gaston KJ. Functional diversity: back to basics and clearly correlated (Table S2), the link between functional di- looking forward. Ecol Lett. 2006;9:741–58. This article intro- duces the concept of functional diversity. versity metrics and landscape change may itself be irrelevant. 6. Petchey OL, Gaston KJ. Functional diversity (FD), species richness Unless the association between functional metrics and ecosys- and community composition. Ecol Lett. 2002;5:402–11. tem functioning is clearly established, it is more likely that 7.� Mouchet MA, Villéger S, Mason NWH, Mouillot D. Functional functional diversity is related to ecosystem functioning diversity measures: an overview of their redundancy and their abil- through a BEF relationship. To fully comprehend which func- ity to discriminate community assembly rules. Funct Ecol. 2010;24: 867–76. This article provides an overview of functional diversi- tions species perform within tropical ecosystems, and how this ty metrics. fluctuates with landscape change and configuration, we sug- 8. Hoehn P, Tscharntke T, Tylianakis JM, Steffan-Dewenter I. gest that further research is needed to establish the connection Functional group diversity of bee pollinators increases crop yield. between landscape changes, functional traits and ecosystem Proc R Soc B Biol Sci. 2008;275:2283–91. 9. Magioli M, Ribeiro MC, Ferraz KMPMB, Rodrigues MG. functioning. If these potentially powerful tools are found to be Thresholds in the relationship between functional diversity and a good proxy for important ecosystem services, the employ- patch size for mammals in the Brazilian Atlantic Forest. Anim ment of these methods in conservation planning and strategy Conserv. 2015;18:499–511. could be invaluable. 10. Leal IR, Filgueiras BKC, Gomes JP, Iannuzzi L, Andersen AN. Effects of habitat fragmentation on ant richness and functional com- Funding Information Funding was provided by NERC grant NE/ position in Brazilian Atlantic forest. Biodivers Conserv. 2012;21: K016393/1 to C.B.L and J.H.H and NERC PhD studentship to 1687–701. M.L.K.H. This paper represents a contribution to the Grand Challenges 11. Magnago LFS, Edwards DP, Edwards FA, Magrach A, Martins SV, in the Ecosystem and Environment Initiative of Imperial College. Laurance WF. Functional attributes change but functional richness is unchanged after fragmentation of Brazilian Atlantic forests. J Ecol. 2014;102:475–85. Compliance with Ethical Standards 12.�� De Coster G, Banks-Leite C, Metzger JP. Atlantic forest bird com- munities provide different but not fewer functions after habitat loss. Conflict of Interest On behalf of all authors, the corresponding author Proc R Soc B Biol Sci. 2015;282:20142844. 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Current Landscape Ecology Reports
– Springer Journals
Published: Mar 28, 2018