Material and methods Study site
Hypothesis 3: Are differences in species diversity and functional rates the
larg-est between the two extremes of habi-tat disturbance?
While we a priori predicted that differ-ences in community composition and func-tional rates would be the most pronounced between the most heavily-modified habitat (banana plantations) and the primary forests, no such pattern appeared. In fact, all baits were removed at a higher rate in banana plan-tations than in primary forests, except for seed
baits in 2013 – but these differences were non-significant. Primary forests had a higher number of ant individuals than banana planta-tions for all bait types in 2013, except for 2011 seed baits (Table S1). However, banana plan-tations overall showed consistently the lowest species richness for both sampling years. For 2011 seed baits, overall species abundance was higher in banana plantations with the most abundant species Pheidole sp.6 (Table S2). In banana plantations, seven primary for-est species were absent, but the same
from primary forests. No difference in species composition between banana and primary forests was statistically significant.
Table 2. Log-likelihood tests of differences in bait removal among sampling years and bait types.
Bait
type 2011 2013
Seeds χ2(2) = 1.579, p = 0.45
χ2(2) = 4.94, p = 0.08 Fish Not measured χ2(2) = 1.9,
p = 0.39 Honey Not measured χ2(2) = 1.02,
p = 0.6
Discussion
It has been suggested that secondary forest could act as a refuge for biodiversity (Wright and Muller-Landau 2006), but less is known about whether such habitat can sup-port imsup-portant ecosystem functions. In this paper, we empirically tested how the compo-sition of ant communities and the ecological functions sustained by ants might change un-der habitat modification in Madagascar. Over-all, we found no clear differences in either community composition or functional rates between three differentially-disturbed habitats.
Below, we will examine these findings in de-tail.
Fig. 4. Fitted means from the models represented in Table 2. Shown is the rate of bait removal in three dif-ferent habitats for each bait type separately: A) seed bait in 2011, B) seed bait in 2013, C) fish bait in 2013 and D) honey bait in 2013. The y-axis represents the fitted means from the model (black dots) for the bait amount (g) removed in 2013 and the number of seeds removed in 2011 with their 95% confidence intervals (vertical lines). Shown on the x-axis are three habitat types (primary forest, secondary forest, and banana plantation). Note that the GLMM models (Tables 1 and 2) revealed no significance differences in bait re-moval between any of the habitat types or years.
17.5 20.0 22.5 25.0 27.5
Primary forest Secondary forest Banana
Fitted mean of seeds removed 2011
0.00 0.05 0.10 0.15 0.20
Primary forest Secondary forest Banana
Fitted means for seed bait (g) 2013
0.2 0.3 0.4
Primary forest Secondary forest Banana
Fitted means for fish bait (g) 2013
0.05 0.10 0.15 0.20
Primary forest Secondary forest Banana Habitat type
Fitted means for honey bait (g) 2013
GLMM, χ2(2) = 1.579, p = 0.45 GLMM, χ2(2) = 4.94, p = 0.08
GLMM, χ2(2) = 1.90, p = 0.39 GLMM, χ2(2) = 1.02, p = 0.60
A B
C D
Hypothesis 1a: Does species richness differ between habitats?
While comparing three habitats differing substantially in their disturbance regime, we detected no clear differences in species rich-ness between habitats. What should be noted is that most of our accumulation curves were quite step, and far from reaching an asymp-tote. This indicates that our sampling effort failed to capture all species present in the habitat and that we may have missed a yet-unknown proportion of rarest species. What we also note is that our current sampling methods may not have yielded a full represen-tation of species diversity in all habitats; as baited traps tend to attract more generalist than specialist ant species (Bestelmeyer et al.
2000). Thus, a full representation of the spe-cies complement would require a very large sampling effort as implemented with a range of techniques. What was still evident was that species accumulated at a very similar rate in the different habitats, offering no indication of differences in the relative dominance of spe-cies, or of consistent differences in species richness among samples of comparable size.
Given no clear-cut evidence for differ-ences in species diversity, our results support evidence from previous studies demonstrating high species richness and abundance of ants in moderately (Dunn 2004, Widodo et al. 2004, Luke et al. 2014) or even highly disturbed hab-itats (Guénard et al. 2015), large forest frag-ments (Vasconcelos et al. 2006) and early successional sites (Palladini et al. 2007). Yet, other studies have reported drastic declines in ant communities, suggesting that it might take up to 100 years for ant communities in dis-turbed habitats to recover to their original state (Bihn et al. 2008). Nonetheless, the study by Bihn et al. (2008) was conducted in an ex-tremely-disturbed habitat: previous pasture. In our study, the secondary forest habitats were never heavily deforested, and the banana plantations examined were close to secondary or even a primary continues forest. Thus, our findings seem to agree with earlier sugges-tions that even small fragments of natural vegetation within agriculture landscapes can sustain high ant species diversity (Pacheco et al. 2013).
Hypothesis 1b: Does species composi-tion and/or abundance differ between habitats?
Our study resolved no significant differ-ences in community composition between the habitats. This concerned both species identity and abundance. In terms of species identity, disturbed habitats hosted 87% of all species detected in the primary forests in 2013 and 90% in 2011. Thus, our results agree with those of Woodcock et al. (2011), who found that while the species composition of a twice-logged forest was slightly altered, 80% of species remained the same as those encoun-tered in an unlogged forest. In terms of overall abundance, we found no significant differ-ences between the habitats.
The similarity in species composition between habitats in our study may be attribut-ed both to a low initial disturbance level and to quick recovery from the disturbed condition.
Most of the secondary forest sites included in our study are currently included in the national park. In terms of recovery, secondary habitats of the tropics quickly reach a complex struc-ture (Guariguata and Ostertag 2001). Studies on other insect group demonstrated that spe-cies composition recovers fast with the regrow of secondary vegetation (Quintero and Roslin 2005). Also for ants, several studies have demonstrated that ant species richness and abundance recover quickly in secondary habi-tats (Widodo et al. 2004), within a time frame of approximately 20-40 years (Dunn 2004).
Finally, due to logistic constraints, the sites examined by us were relatively close to each other and to primary forests (Fig. 1), thus po-tentially providing source populations of most species to sustain a population in secondary habitats.
Highly and moderately disturbed habi-tats had lost some of the primary forest spe-cies but gained some spespe-cies not observed in primary forests. However, the abundance of these species was low and these differences could thus be attributed to sampling effects alone. Some other species occurring in all three habitats also seemed to consistently increase in abundance in secondary forests or banana plantations. Whether or not some of these species may be seen as invasive is so far unknown. The frequent occurrence of a widespread invasive ant Pheidole megacepha-la (Fabricius, 1793) and other invasive Phei-dole species in Madagascar (Fisher and Fisher
2013) suggests that some of the Pheidole ants currently identified to the level of morphospe-cies could potentially represent invasive taxa.
However, the present level of identification does not suffice to establish whether this is the case. Tetramorium simillimum (Smith, 1851) was another invasive ant species de-tected in low abundance in banana plantations in 2011, whereas no other species detected in banana or secondary forests appeared inva-sive.
Hypothesis 2: Does the rate of ecosys-tem functions differ between habitats?
Our assessment of proxies for three dif-ferent ecological functions offered no proof for differences in rate between habitats. Overall, the rate of bait removal was more reflective of the bait type itself than of the habitat type in which it was offered. Whatever pattern emerged in one year was also inconsistent in time. For example, removal of seed bait showed different patterns between the two sampling years. In 2011, we saw more seed non-significant but marginally lower in primary for-ests than in secondary forfor-ests. The lack of differences in ant-sustained functions be-tween habitats conforms to the lack of pat-terns reported by (Philpott et al. 2008) for ant predation in different-intensity coffee planta-tions. Thus overall, there seems to be no clear indication of an association between moderate habitat disturbance and the rate of ecological functioning as sustained by ants.
Hypothesis 3: Are differences in species diversity and functional rates the larg-est between the two extremes of habi-tat disturbance?
Contrary to priory expectations, we found no consistent differences in species diversity or functional rates between the two extremes of habitat disturbance – i.e. primary forests and banana plantations. This lack of patterning contrasts with previous studies demonstrating that high disturbance reduces species diversity (Philpott and Foster 2005).
Such patterns have been attributed to a re-duction in the availability of nesting sites with simplified habitat structure (Philpott and
Foster 2005). Nonetheless, in our study, the lack of differences between habitats appeared highly consistent. First, the same lack of de-tectable effects was observed for all three proxies of functioning measured: seed remov-al, predation and ant-Hemiptera mutualism.
Second, the lack of significant patterns within years was matched by inconsistency in the slight but non-significant patterns between years. This adds credence to the true lack of an effect.
Conclusions
Overall, the lack of consistent differ-ences between habitats in terms of both ant community structure and in the rate of ecolog-ical functions sustained by ants offer a hope-inspiring message: maybe ant assemblages are relatively resilient to moderate habitat modification? Nonetheless, great care needs to be taken before the current findings are extrapolated to any setting beyond the current one. What we clearly cannot say is whether there are tipping points in disturbance versus function beyond the current disturbance lev-els, as our study only spanned a limited range of disturbance regimes. Likewise, we stress that our findings may be conditional on the structure of the landscape where our study was conducted. Within the protected areas of the Ranomafana National Park, there is a con-tinuous proximity of source populations, the impact of which we have not established.
Having said all this, there is no reason not to grasp the suggestion of positive news, too. As secondary habitats are becoming a common landscape feature (Guariguata and Ostertag 2001), the conservation of such habi-tats might be a useful management strategy from the perspective of conserving ant diversi-ty. All taxa may not equally sensitive to habitat disturbances, and several researchers (e.g.
Dunn 2004, Quintero and Roslin 2005, Vasconcelos et al. 2006, Luke et al. 2014), demonstrated that even insect groups differ from each other in how they react to habitat disturbance. Maybe some ants fall among the more resilient end of this spectrum? To find out, more research of the current kind is ur-gently needed, ideally encompassing further functions in further habitat types.
Acknowledgements
The Academy of Finland supported this research with grant number 250444 (to Mar Cabeza). Silvija Budaviciute received individu-al grants from the Otto. A. Mindividu-alm Foundation, the Oskar Öflund Foundation, Societas Ento-mologica Helsingforsiensis (2011 and 2012) and Societas Entomologica Fennica (2014).
This work would not be possible without the technicians in Madagascar François Ratalata, Albert Telo and August Pela, volunteers Riikka Kinnunen, Aurora Paloheimo and Akvilė Norkutė. We also thank field assistants Sa-hondra Lalao Rahanitrinianina, Jocelyn Ma-miarilala and Rakoto Nirina. Thank you Anta-nanarivo Biodiversity Centre and especially Balsama Rajemison for her help and lending us some of the fieldwork equipment. SB is grateful to Brian L. Fisher for hosting her at the California Academy of Sciences while she was learning to recognize different ant species.
Dmitry Dubovikoff provided valuable com-ments and advice on ant identification during his visiting to the Museum of Natural History in Helsinki, whereas F. Guillaume Blanchet pro-vided valuable comments on the methods.
Erin Cameron offered valuable improvements to an earlier version of the manuscript. Re-search, collecting and export permits were obtained through collaboration with the "Min-istère de l' Environnement et des Forêts", In-stitut pour la Conservation des Environments Tropicaux (MICET) and the Madagascar Na-tional Parks.
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