Recolonization of mollusc assemblages in mangrove plantations damaged by Typhoon Chan-hom in the Philippines

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Highlights

  • Severe damage to vegetation structure and sediment properties (associated with a reduction in tree density and canopy cover resulting in increased temperatures and exposure) following the typhoon resulted in an alteration of trajectory patterns in the damaged stands.

  • There were shifts in species composition and dominant species from having mature mangrove-associated species (pre-typhoon) to an abrupt return in dominance of pioneer species (post-typhoon).

  • The reduced presence and activities of molluscs (i.e. as bioturbation) may have contributed to the delayed recovery of mangroves.

Abstract

We investigated the effects of a catastrophic typhoon on mollusc assemblages of damaged mangrove plantations of different ages. Molluscs were sampled from infaunal, epifaunal and arboreal assemblages of mangrove stands in Lingayen Gulf, northwest Philippines, and compared with assemblages of un-impacted areas. Prior to the occurrence of the typhoon, there were clear shifts in the species diversity (H’) and composition of mollusc assemblages with stand age of mangrove forests. This was observed in species composition through the succession in dominance from pioneer to seral or putative climax species, and assemblage type (as arboreal, epifaunal and infaunal). However, severe damage to vegetation structure and sediment properties (associated with a reduction in tree density and canopy cover resulting in increased temperatures and exposure) following the typhoon resulted in an alteration of trajectory patterns in the damaged stands. There were shifts in species composition and dominant species from having mature mangrove-associated species (pre-typhoon) to an abrupt return in dominance of pioneer species (post-typhoon). The damage was more evident in older stands than in intermediate-aged stands. Furthermore, the reduced presence of molluscs (and also probably their activities, i.e. burrowing) may have contributed to the delayed recovery of mangroves. The prospects for recovery of the system to pre-typhoon levels are therefore uncertain where the re-establishment of seral or edaphic mollusc assemblages appears to be related to the recovery of vegetation and sediment conditions.

Introduction

Mangrove restoration (mainly through plantation) has been a popular resource management program in the Philippines since the late 1980s (Salmo et al., 2007). Mangrove planting has been widely practiced in most parts of the country and gains community support because of the employment that it provides to locals. Aside from the main objectives of restoring forest cover and providing protection from typhoons, mangrove planting is also used to enhance coastal fisheries production. Among fisheries products expected to be derived from mangrove plantations are nekton (especially fishes, crabs and shrimps) and molluscs (Salmo et al., 2018).

Upon growth of replanted mangroves, their forest structure becomes more complex, and increasing amounts of detritus are produced, providing food and habitat for various organisms (see reviews by Cannicci et al., 2008; Nagelkerken et al., 2008). Patterns of changes in the density, biomass and species composition of the fauna are expected to occur as the forest vegetation changes with stand age. Among mangrove-associated faunal groups, molluscs are one of the more conspicuous organisms. Changes in the mangrove community will likely influence shifts in species composition, abundance, and biomass of the mollusc assemblage (Sasekumar and Chong, 1998; Netto and Galucci, 2003) and will vary with assemblage types (from infauna to epifauna and arboreal). We adapted the definitions of assemblage types as infauna (molluscs inside the sediment), epifauna (molluscs on the sediment surface), and arboreal (molluscs attached to the mangrove stems and prop roots; cf. Salmo et al., 2017). Other factors that are known to affect the distribution and composition of benthic fauna (e.g., physical attachment, structural complexity, tidal elevation) have been assessed in several studies (see Kathiresan and Bingham, 2001; Chapman and Tolhurst, 2007; Nagelkerken et al., 2008 inter alia). The role of forest cover in mollusc abundance and biomass has been emphasized by Fondo and Martens (1998) and Sasekumar and Chong (1998).

This notable dependence of mollusc fauna on habitat condition leaves them vulnerable to severe disturbance events like typhoons. Typhoons are natural disturbances that frequently occur especially in the tropics. In the Philippines, around 20 typhoons occur each year, with intense events (>150 km h−1) having 16–32 years oscillation (Kubota and Chan, 2009). The particularly severe typhoons bring strong winds, intense rainfall and large storm surges causing notable damages to the environment, property and human lives, particularly in coastal areas (Cinco et al., 2016). These larger typhoons are known to cause significant reductions in mangrove forest cover as well as an associated loss of organic matter in sediments (Salmo et al., 2014). However, the extent and scale of damage within a forest stand are heterogenous and vary with wind speed and localized site gradients such as geographical position relative to shoreline and tree height (Everham and Brokaw, 1996; Busby et al., 2008). Mangrove plantations are perceived to be more vulnerable than natural stands because of their lower structural complexity and lower wind firmness (cf. Gardiner and Quine, 2000).

There is an acknowledged need to investigate the colonization by molluscs in mangrove forests damaged by typhoons. Prior to the typhoon, we reported a clear trajectory of mollusc colonization and shift of dominant species as well as assemblage type (from arboreal to epifauna to infauna) with age of the stands (Salmo et al., 2017). Such shifts are correlated with the changes in vegetation and sediment conditions primarily with canopy cover and biomass (for the vegetation) and OM (in the sediments). Some species dominate in young plantations (<10 years; Pirenella cingulata) and in intermediate-aged plantations (10–15 years; Nerita polita), while other species are known to occur most in mature (>15 years) and natural stands (Terebralia sulcata; Nerita planospira). The species P. cingulata and N. polita dominates in infaunal and epifaunal assemblages while T. sulcata and N. planospira are more prominent in arboreal assemblage. Catastrophic typhoons are likely to contribute to reductions in habitat quality as well as a decrease in the supply of food for molluscs. An alteration of mollusc colonization pattern but more particularly a shift in dominant species (e.g. reverting from pre-typhoon mangrove-associated species to post-typhoon pioneer species in mature plantation) may commence after drastic changes in vegetation and sediment conditions. Smith et al. (1994) stressed however that the effects of such severe disturbances on the recruitment and colonization dynamics of mangrove-resident fauna had not been adequately studied.

When severe Typhoon Chan-hom struck Lingayen Gulf in northwestern Philippines on 9th May 2009 affecting our established study sites, we took the opportunity to test the hypothesis that mangrove habitat degradation caused by severe typhoons might influence and possibly disrupt the colonization and restoration of mollusc assemblages. The following account documents our subsequent findings on the effects of Typhoon Chan-hom on the recolonization of mangrove mollusc assemblages (from arboreal to epifaunal and infaunal assemblages) in mangrove plantations in the Philippines. Based on these new observations, we provide a re-evaluation of the possible role of molluscs in the post-disturbance recovery of mangrove habitat.

Section snippets

Site description

The study was conducted in Rhizophora mucronata plantation stands of different ages in Lingayen Gulf, northwestern Philippines (Fig. 1). These plantation plots (codes in brackets) were: in Tondol, Anda (6 years – labelled as P6); Mona, Alaminos (8 years – P8); Imbo, Anda (10 years – P10); Pilar, Bolinao (11 years – P11); and Bangrin, Bani (18 years – P18). Mangrove plantations in Alaminos, Anda and Bolinao are more exposed to coastal processes, while those in Bani are located in sheltered areas

Pre-vs post-typhoon changes in arboreal assemblage

A total of 10,625 individuals composed of 28 species from 16 families were recorded, of which the majority were gastropods (97 %; Supplemental Table 1). There were no significant differences in mollusc biomass among mangrove stands throughout the sampling periods, largely because of the high variability in each site. Prior to the typhoon, the pooled samples from each developmental stage yielded significant correlation between forest stage and biomass (Y = 88.603 ln (x) – 122.67; r2 = 0.61).

Discussion

A total of 38 species from 23 families were collected from all sites which is comparable to the mature and natural Rhizophora mangroves in SE Asia (see Salmo et al., 2017) – 26 in natural stands in Selangor, Malaysia (Sasekumar, 1974), 34 in natural and planted mangroves in Ranong, Thailand (Macintosh et al., 2002), and 44 in nearly pristine mangroves in Sarawak, Malaysia (Ashton et al., 2003). Consistent with published reports, only a few taxa (at most 5–9) dominate at each site (Sasekumar,

Conclusions

A catastrophic typhoon resulted in the alteration of the restoration trajectory of mollusc assemblages. But the damage was more evident in more mature stands than in intermediately old stands. Post-typhoon changes in mollusc assemblages were attributed to the sudden reduction or loss of their sources of habitat and food. Shifts in dominant mollusc species from pre-typhoon to post-typhoon in all assemblages were attributed to changes in vegetation and sediment conditions. Moreover, the severe

Acknowledgment

The Ford Foundation International Fellowship Program, the International Foundation for Science (D/4667-1), and the University of Queensland Research Scholarship Grant provided funding to SS. Staff of the University of the Philippines Marine Science Institute (particularly in the Bolinao Marine Laboratory) assisted and provided SS laboratory space in Bolinao. Jack Rengel and Ruel Conzaga assisted in the field sampling. The authors thank the local government units and mangrove managers from all

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