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Article

Potential Detritivorous Diet of the Invasive Apple Snail (Pomacea canaliculata Lamarck, 1822) in Mangroves: The Relationship between Feeding Indicators and Chemical Characteristics of Decaying Leaf Litter

by
Jinling Liu
1,
Zhihua Chen
1,
Yunhui Li
1,
Danying Chen
1,
Yulin He
1,
Benliang Zhao
2,*,
Yuexin Liao
1 and
Jing Guo
3
1
College of Biology and Food Engineering, Guangdong University of Education, Guangzhou 510303, China
2
Heyuan Branch, Guangdong Laboratory for Lingnan Modern Agriculture, College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China
3
Henry Fok School of Biology and Agriculture, Shaoguan University, Shaoguan 512005, China
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2023, 11(3), 672; https://doi.org/10.3390/jmse11030672
Submission received: 2 February 2023 / Revised: 10 March 2023 / Accepted: 13 March 2023 / Published: 22 March 2023
(This article belongs to the Section Marine Biology)
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Abstract

:
Invasive species have had substantial impacts on global mangrove forests. Apple snails (Pomacea canaliculata) have invaded mangrove forests in China. To clarify the potential detritivorous diet of P. canaliculata, the growth and feeding indicators of invasive juvenile snails collected from mangroves in Guangzhou, China, were studied using decaying leaf litter from five mangrove species, including Acanthus ilicifolius, Acrostichum aureum, Kandelia candel, Aegiceras corniculatum, and Sonneratia apetala. The growth indicators of the survival ratio and specific growth rate were calculated by measuring the live weight of the snails and the number of dead snails after 30 days. The feeding indicator of the weight-specific daily feeding rate (WDR) was calculated by measuring the snail weight and the amount of leaf litter ingested after 120 h. A multiple-choice experiment was performed on the snails by providing the decaying leaf species together, while a no-choice experiment was performed using a single species of decaying leaf litter. The survival and specific growth ratio of P. canaliculata feeding on decaying leaf litter of A. ilicifolius were higher than those for A. aureum. The WDR values of P. canaliculata feeding on the decaying leaf litter of A. ilicifolius and S. apetala were both significantly higher than those for A. corniculatum, A. aureum, and K. candel. The lowest WDR value of P. canaliculata feeding on decaying leaf litter was observed for A. aureum in the no-choice experiment. P. canaliculata mainly fed on decaying leaf litter of A. ilicifolius and S. apetala. The phosphorous contents and ash of the decaying leaf litter positively affected the WDR values of P. canaliculata obtained in the multiple-choice and no-choice experiments. The contents of lignin, tannin, and flavonoid negatively affected the WDR values of P. canaliculata. The potential diet of invasive P. canaliculata in mangroves was closely tied to the chemical characteristics of the decaying leaf litter. P. canaliculata can invade A. ilicifolius and/or S. apetala mangroves by utilizing the debris on the mangrove ground. Understanding the potential detritivorous diet of P. canaliculata in invaded mangroves can help us to assess this species’ dispersal risk and provide support for mangrove management.

1. Introduction

Mangroves are coastal ecosystems with the highest level of primary productivity in (sub)tropical intertidal areas, with a global distribution of 130,000–150,000 km2 [1,2]. In addition to being significantly productive ecosystems worldwide, mangrove forests exhibit multiple ecosystem services, including the maintenance of diverse habitats for coastal creatures [3], nutrient sink [4], carbon storage [5], coastline protection, and disaster mitigation [6].
As a woody plant community located in the intertidal zone, the biomass of mangroves has been significantly disturbed by both natural and anthropogenic stressors on a global scale [7]. Similar to many other ecosystems, mangrove forests are also emerging hotspots of invasion by exotic species due to the complex habitats they hold [8]. Invasive species, especially animals, have significantly or potentially influenced mangroves by means of voracious appetites [9], interspecific competition [10], predation [11], nutrient cycle interruption [12], and habitat modification [13].
Ecological and socio-economic services dependent on mangrove ecosystems have been profoundly impacted by invasive species. A fundamental step in the risk assessment and effective control of invasive species is to determine their role in the food chain in mangroves. Mangrove litter fall is an essential link in the mangrove food chain. The litter fall values of mangroves range from 1.66 to 28.81 Mg−1 ha−1 yr−1 across the neotropics [14]. As an essential food source for benthic animals, mangrove litter largely dominates the structure of the benthic food web in mangrove forests [15]. However, mangrove litter simultaneously offers advantages for the intrusion and establishment of invasive species. For example, the detritus of mangrove Barringtonia racemosa leaves contributes 30% of the diet of the invasive snail Tarebia granifera [16].
Apple snail (Pomacea canaliculata Lamarck, 1822), a harmful freshwater gastropod, is listed as one of the 100 worst invasive alien species [17]. P. canaliculata is native to South America and has observably threatened rice productivity in Asia by directly feeding on rice seedlings [18]. P. canaliculata is also a crucial vector of the parasitic nematode Angiostrongylus cantonensis, which causes rat lungworm disease in humans in Asia [19]. P. canaliculata has established populations in diverse aquatic habitats in Asia, North America, South America, and Oceania and shown a tendency to genetically adapt to the climate and agricultural activities of the areas it occupies [20].
Although P. canaliculata is a freshwater snail, one study reported a population of this species in a Chilean lagoon with low salinity (1–2.1 ppt) [21]. A laboratory study confirmed that this species could survive in brackish water (5 ppt) [22]. Due to its ability to resist saline stress and a diverse range of microhabitats in mangrove forests [23], this species can invade mangrove forests. In 2018, a benthic investigation found that this species had invaded mangroves in the National Wetland Reserve on Hainan island, China [24]. In 2019, researchers discovered that P. canaliculata had invaded mangrove forests in Nansha District, Guangzhou city, China (Supplementary Figure S1) [25].
However, the characteristics of the food source of P. canaliculata in mangrove forests remain to be determined in detail. A previous study discovered that the leaves of a mangrove species known as Acanthus ilicifolius L. could effectively sustain the proliferation of adult P. canaliculata compared with another four species, including Acrostichum aureum L., Kandelia candel L., Aegiceras corniculatum L., and Sonneratia apetala Buch.-ham. Such a phenomenon suggests that mangrove leaf litter may facilitate the population establishment of P. canaliculata in mangrove forests. Most mangrove leaf litters are sturdy and hard to digest due to their high C: N ratios and concentrations of anti-nutritional secondary compounds that inhibit digestion [26]. Although such traits of leaf litter, to some extent, can protect mangrove forests from the invasion of P. canaliculata, the decaying process of the litter may weaken this barrier. The secondary anti-nutritional metabolites contained in leaf litter, especially tannins, saponins, alkaloids, and phytates, can slowly decrease due to the decay process of fragmentation, breakdown, leaching, and degradation of refractory components in leaf litter on the forest floor [27,28,29]. In addition, many researchers have reported that juvenile mangrove snails are detritivorous and shift their diets to meet their nutrient demands during development [30,31]. Considering the omnivorous appetite of P. canaliculata [32], we speculated that the decaying leaf litter could represent a critical step in the establishment of P. canaliculata in an unfavorable type of mangrove. However, little is known about the feeding behavior of P. canaliculata on decaying mangrove leaf litter. In light of such a scenario, we posed three questions: (1) Can the juvenile P. canaliculata grow on the decaying leaf litter of mangroves? (2) Have juvenile P. canaliculata a feeding preference for decaying leaf litter of different mangrove species? (3) Do the chemical properties of decaying mangrove litter affect the preference of juvenile P. canaliculata? The resolution to these questions would help to clarify whether P. canaliculata can survive in mangrove forests and understand its potential detritivorous diet. This research can also help us to assess the risk of invasive snails in mangroves and support mangrove management efforts.

2. Materials and Methods

2.1. P. canaliculata and Decaying Leaf Litter

The tested juveniles were the progeny of apple snails, which were collected from the mangrove forests in Guangzhou, China (22°62′ N, 113°66′ E), in February 2019. The mean air temperature and the annual precipitation in the sampling region from 2019 to 2021 were 24.2 °C and 1677.3 mm [33]. The parental snails collected from the field location were identified as P. canaliculata (GenBank accession numbers: MW799954, MW799955 [25]).
Hatched P. canaliculata juveniles aged over two weeks old were reared in artificial seawater (3 ppt) in aquaria (80 cm × 60 cm × 60 cm) at a water temperature of 25 ± 1 °C and pH (7.3–7.5) based on the water quality of the sampling locations [25]. The artificial seawater in the aquaria comprised aerated tap water and was refreshed every day. The salinity was adjusted by supplying artificial sea salt (Yanzhibao, Guangdong, China), which was measured with a salinity meter (Shanghai Sanxin Instrument Co., Ltd., SX5051, Shanghai, China). Before the experiment, the juveniles were fed with lettuce (Lactuca sativa L.) every day at the same temperature (25 ± 1 °C). Healthy snails were used in the experiments. These healthy snails had the characteristic of smooth and intact shells, and they were in an active state, characterized by continuous movement in the aquaria. Juvenile snails that did not reach sexual maturity were used in the experiments [34]. After being starved for 24 h, the snails were used in experiments conducted at room temperature (25 ± 1 °C) in seawater (3 ppt).
The leaf litter of five mangrove species was used to determine the growth and feeding indicators of P. canaliculata. The tested mangrove species included Acanthus ilicifolius L. (Acanthaceae, holy mangrove shrub), Acrostichum aureum L. (Pteridaceae, mangrove fern), Kandelia candel L. (Rhizophoraceae, narrow-leaved Kandelia), Aegiceras corniculatum L. (Primulaceae, black mangrove), and Sonneratia apetala Buch.-ham (Sonneratiaceae, mangrove apple) [25].
We used plastic nets (<0.850 mm) to collect fallen leaf litter from the mangrove forest. The collected leaf litter was composed of naturally fallen leaves accumulated on the same day without human interference. Leaf litters of similar sizes were selected to ensure that they had similar physical and chemical characteristics in the experiments. We used a burying treatment to obtain the decaying mangrove leaf litter [26]. A plastic box was filled with mangrove sediments (depth 15 cm) collected from the mangrove forest. The leaf litter (50 g ± 1 g) was placed in a net bag with a rope (30 cm × 20 cm, 5 mm mesh) before being buried at a 5 cm depth from the sediment surface. The level of artificial seawater (3 ppt) was maintained daily at 5 cm, and the seawater was replaced every 5 days before retrieving the litter bags after 30 days. The leaf litter was carefully cleaned using purified water to remove adhered salts, sediment particles, and microfauna. Part of the leaf litter was measured for its moisture content by oven drying at 105 °C (4 h) and 80 °C (48 h) to a constant weight [25]. The left leaf litter was stored at 4 °C in the refrigerator for further experiments.
The chemical characteristics of the decaying leaf litter, including the contents of carbon, nitrogen, phosphorous, calcium, protein, ash, fiber, lignin, tannin, phenol, and flavonoid, were determined according to the method of [35,36,37,38,39,40,41] (Table 1).

2.2. Growth of P. canaliculata Feeding on Decaying Leaf Litter

Five species of decaying mangrove leaf litter were separately placed in a chamber (25 cm diameter × 10 cm height) together with ten healthy snails (height: 1.42 ± 0.03 cm) [25]. The decaying leaf litter (5.0 g) and the seawater (4 L, 3 ppt) in each chamber were refreshed daily. The decaying leaf litter was cleaned with filter paper before use. The growth experiment was performed in 4 replicates for each kind of decaying leaf litter and lasted for 30 days. The initial live weight (LW1, g) and the final live weight (LW2, g) of the snails were measured using an electronic balance [25]. The specific growth rate (%·d−1) of the snails was calculated as (lnLW2 − lnLW1)/30 × 100% [42]. The number of dead snails was checked and recorded daily [18]. According to the accumulated quantities of dead snails (AQ), the survival ratio was calculated as (10 − AQ)/10 × 100% after 30 days. Dead snails were taken out of the chamber during each check. The removal of dead individuals did not affect the diet of the surviving juveniles because enough decaying leaf litter and the same water quality were provided in the chamber.

2.3. Multiple-Choice Experiment of P. canaliculata on Decaying Leaf Litter

Another experiment was conducted to measure the preference of P. canaliculata for five kinds of mangrove decaying leaf litter under multiple-choice feeding conditions [25,43]. The mangrove decaying leaf litter was cleaned with purified water before use. Each kind of decaying leaf litter weighed from 0.9 to 1.1 g. Decaying leaf litter (5.0 g) from five mangrove species was placed in a chamber (25 cm diameter × 10 cm height) filled with artificial seawater (4 L). P. canaliculata, with a height of 1.40 ± 0.03 cm, were then placed in the chamber. The artificial seawater (3 ppt) was refreshed every day. The experiment was performed in four replicates. After 120 h, the remaining mangrove decaying leaf litter was oven-dried at 105 °C (4 h) and 80 °C (48 h) to a constant weight after removing the adhered salt using purified water [25]. All the individuals were alive during the 120 h of the experiment.

2.4. No-Choice Experiment of P. canaliculata Feeding on Decaying Leaf Litter

Another experiment was conducted to measure the palatability of five kinds of mangrove decaying leaf litter to P. canaliculata under no-choice feeding conditions [25]. The mangrove decaying leaf litter was cleaned using purified water before use. Ten healthy snails with a height of 1.40 ± 0.02 cm were placed in a plastic chamber (25 cm diameter × 10 cm height) together with a species of decaying leaf litter (5.0 g) after the recording of their live weights. Plastic chambers with artificial seawater (4 L, 3 ppt) were used in the experiment. All the individuals were alive after 120 h. The artificial seawater in each chamber was refreshed every day. The experiment was performed in four replicates. After 120 h, the remaining mangrove decaying leaf litter was oven-dried at 105 °C (4 h) and 80 °C (48 h) to a constant weight after removing the adhered salt using purified water [25].

2.5. Feeding Indicators of P. canaliculata

The amount of leaf litter ingested was calculated according to the initial and final dry weights. The initial dry weight of the leaf litter of five species of mangroves was obtained according to the fresh weight used in the multiple-choice and no-choice experiments and the moisture content. After 120 h of the multiple-choice and no-choice experiments, the final dry weight of the remaining mangrove decaying leaf litter was measured by drying at 105 °C (4 h) and 80 °C (48 h) to a constant weight. The remaining decaying leaf litter was rinsed and cleaned to remove the adhered salt. The weight-specific daily feeding rate (WDR) was used to analyze the feeding behaviors of P. canaliculata under the multiple-choice and no-choice feeding conditions, according to Equation (1).
W D R ( g ⋅ g ⋅ h − 1 ) = amount   of   leaf   litter   ingested weight   of   ten   snails × 1 120

2.6. Statistical Analyses

We performed all statistical analyses using R software 4.0.3 [44]. To compare the growth and feeding indicators of P. canaliculata on decaying leaf litter, the Kolmogorov–Smirnov test and Levene test were used to analyze the normality and homogeneity of variances of the data. We used ANOVAs (Tukey) and nonparametric tests (Kruskal–Wallis with Dunn–Bonferroni) to compare the feeding indicators of P. canaliculata for decaying leaf litter. We performed a collinearity test of the variables through the R package “vegan” [44,45,46]. To analyze the correlation between the feeding indicators and chemical characteristics of decaying leaf litter, we used Pearson’s correlation, linear fit, and redundancy analyses (RDA), implemented through the R packages “stats”, “vegan”, “ggplot2”, and “ggrepel” [44,46,47,48]. We used principal component analysis (PCA) implemented through the R packages “FactoMineR” and “factoextra” to further analyze the clustering of the feeding indicators of P. canaliculata on decaying leaf litter [44,49,50].

3. Results

3.1. The Growth of P. canaliculata on Decaying Leaf Litter

The specific growth ratios of P. canaliculata feeding on decaying leaf litter of A. aureum, K. candel, and A. corniculatum had negative values. The average specific growth ratio of the P. canaliculata that consumed the decaying leaf litter of A. ilicifolius was 6.6, 6.5, and 6.5 times as high as the values (absolute values) for A. aureum (p < 0.01), K. candel (p < 0.01), and A. corniculatum (p < 0.01), respectively. The survival ratio of P. canaliculata feeding on A. ilicifolius (p = 0.027) or S. apetala (p = 0.027) litter was significantly higher than that of snails feeding on A. aureum, whereas no significant differences were observed between the decaying leaf litter of A. aureum, K. candel, and A. corniculatum (Figure 1).

3.2. The Feeding Indicators of P. canaliculata on Mangrove Leaves

Under the multiple-choice feeding conditions, the WDR values of P. canaliculata feeding on decaying leaf litter of A. ilicifolius and S. apetala were both significantly higher than those for A. corniculatum, A. aureum, and K. candel (Figure 2A). The lowest WDR of P. canaliculata feeding on decaying leaf litter was observed for A. aureum. The P. canaliculata tended to feed on the decaying leaf litter of A. ilicifolius and S. apetala when the five mangrove species were offered simultaneously. The WDR of P. canaliculata feeding on the decaying leaf litter of A. aureum was less than 0.002.
Under the no-choice feeding conditions, the WDR decreased as follows: A. ilicifolius, S. apetala > A. corniculatum, K. candel > A. aureum (p < 0.05) (Figure 2B). The WDR indicator showed that P. canaliculata mainly fed on the decaying leaf litter of A. ilicifolius and S. apetala when the five kinds of decaying leaf litter were provided independently as food. The median WDR of P. canaliculata feeding on the decaying leaf litter of A. aureum was less than 0.01. This was consistent with the result showing that A. aureum did not sufficiently support the snails’ growth compared with A. ilicifolius and S. apetala used in the growth experiment.

3.3. Correlation Analysis between the Diet and Chemical Characteristics of Decaying Leaf Litter

The feeding indicators showed different relationships with the chemical characteristics of decaying leaf litter in the correlation analysis (Table 2 and Table 3). Under the no-choice feeding conditions, the WDR indicator was significantly positively correlated with the phosphorous content and ash of the decaying leaf litter, whereas a significantly negative relationship was observed between this indicator and the contents of lignin, tannin, and flavonoid. Under the multiple-choice feeding conditions, a positive correlation of the WDR with the contents of nitrogen, phosphorous, protein, and ash was observed, whereas a significantly negative correlation was observed between the WDR and the contents of lignin, tannin, phenolic, and flavonoid.
Significantly positive linear relationships between the indicators of the WDR and WDRN and some of the chemical characteristics of the decaying leaf litter were observed under the multiple-choice and no-choice feeding conditions (Supplementary Tables S1 and S2; Supplementary Figures S3 and S4). Under the multiple-choice feeding conditions, the indicator WDR had a significantly positively linear relationship with the nitrogen, phosphorous, ash, and protein contents (Supplementary Tables S1 and S2). In contrast, the same indicator WDR was significantly negatively linear related to the contents of flavonoid, lignin, phenolic, and tannin (Supplementary Table S2). Under the no-choice feeding conditions, the indicator WDRN showed a significantly positively linear relationship with the phosphorus and ash contents (Supplementary Table S1), whereas it showed a significantly negative linear relationship with the flavonoid, lignin, and tannin contents (Supplementary Table S2).
Based on the collinearity analysis, RDA was performed to distinguish the main factors influencing the feeding indicators of P. canaliculata (Figure 3). The results showed that the ash content in the decaying leaf litter positively influenced the indicators under the multiple-choice (WDR) and no-choice conditions (WDRN). In contrast, the lignin and flavonoid contents were significantly negatively related to the indicators. RDA confirmed that the decaying leaf litters of A. ilicifolius and S. apetala were the preferred foods for P. canaliculata. The chemical characteristics of A. corniculatum, A. aureum, and K. candel were closely related to the contents of lignin and flavonoid, indicating that they were unfavored as food sources by P. canaliculata.
Based on the significantly correlated chemical characteristics of the decaying leaf litter of five species of mangroves, PCA was applied for the feeding indicators of P. canaliculata (Supplementary Figure S2). Principal components 1 and 2 explained 65% and 19% of the total variation (eigenvalues > 1). PCA showed that the decaying leaf litter of five mangrove species formed four clusters, and two mangrove species significantly overlapped.

4. Discussion

4.1. Survival and Growth on Decaying Leaf Litter

As an r-strategist species, P. canaliculata shows typical characteristics of high reproduction [51]. Researchers found that the number of eggs laid by a female P. canaliculata at one time reached 1000 individuals per mass, supporting the successful invasion of a new habitat by this population [52]. Food availability acts positively on the survival of juvenile P. canaliculata. The limited food sources of weed (Lemna paucicostata) and algae (Zygnemataceae) led to a decrease in the survival of P. canaliculata juveniles in a paddy field [53]. In this study, we replaced the decaying leaf litter every day to ensure that enough food supply was provided to the individuals. The results indicated that the decaying leaf litter of A. ilicifolius effectively supported the growth of P. canaliculata juveniles, followed by S. apetala. The survival of P. canaliculata juveniles was also influenced by the species of decaying leaf litter. Furthermore, negative values were observed for the growth of P. canaliculata that consumed decaying leaf litter of A. aureum, K. candel, and A. corniculatum, indicating that the nutrient uptake of the surviving P. canaliculata juveniles consuming decaying leaf litter was insufficient to compensate for their metabolic consumption. Starvation resistance is partly involved in this pattern, as previous research reported that the mortality of juvenile P. canaliculata reached 100% only after 16 days of starvation under moist conditions [54]. The weight of P. canaliculata adults feeding on leaves of K. candel, S. apetala, and A. corniculatum increased, although these mangrove species were not favorable to P. canaliculata adults [25]. Therefore, the digestive capacity or nutrient transform efficiency of P. canaliculata juveniles might be lower than that of adult individuals.

4.2. Feeding Preference of P. canaliculata on Decayling Leaf Litter

P. canaliculata can feed on the leaves of various aquatic plants in freshwater wetlands and mangrove forests [55]. Among these plants, the feeding preference of P. canaliculata feeding on macrophytes has been relatively well studied compared with that of P. canaliculata feeding on mangrove plants. In contrast, there is still much to learn about the feeding preference of P. canaliculata for the decaying leaf litter of mangroves. We found that P. canaliculata could feed on five kinds of decaying leaf litter from mangroves, and two of them (A. ilicifolius and S. apetala) were more preferentially consumed. Such a preference of P. canaliculata for decaying leaf litter possibly resulted in competitive conflict with several native species of leaf litter consumers, primarily crabs and gastropods, in mangrove forests. Juveniles of the snail Terebralia palustris were found to be detritivorous in mangrove forests, and 19% of the juveniles’ gut content was leaf debris [30]. Previous studies have found that P. canaliculata had a higher conversion efficiency than native snails, and it could influence native snails through food source consumption in a shared freshwater habitat [56]. Competition may exist between P. canaliculata and native juvenile snails.
However, the situation may be different for the mangrove crab. A previous study reported that the crab Eriocheir japonicas could be a natural enemy that predates on juvenile P. canaliculata [57]. Meanwhile, the mangrove crab Neosarmatium smithi can compete with the mangrove snails by pulling the decayed leaves away or pushing the snails off the leaves when they are foraging in small habitats, although the latter exhibited aggregation behavior [58]. As P. canaliculata also showed aggregation behaviors [59], the possible interaction of competition or predation between the native mangrove crab and invasive P. canaliculata juveniles requires detailed investigation. Similar to the benthic crab and snails, which frequently feed on the decaying litter of mangroves [30], the consumption behaviors of P. canaliculata on decaying leaf litter could accelerate nutrient release to sediments. However, stable isotopes reveal that microphytobenthos are also primary food sources for the benthic gastropod [60], and the diet of the invasive P. canaliculata feeding on decaying leaf litter might modify the structure of the benthic food chains from a trophic point of view.
The WDR indicator reflected the consumption rate and nutrient uptake efficiency of the decaying leaf litter in relation to the feeding duration and accumulated weight of the snails. Under the multiple-choice and no-choice feeding conditions, the WDR indicator of P. canaliculata showed a significant difference between group A. ilicifolius & S. apetala and group A. corniculatum & K. candel. This phenomenon suggested that the consumption rate and efficiency of nutrient uptake of the snails were different when feeding these species of decaying leaf litter.
Furthermore, we observed a decrease in the WDR of P. canaliculata feeding on the five species of decaying leaf litter under the multiple-choice feeding conditions compared with the no-choice feeding conditions. This phenomenon, possibly due to intraspecific competition between the individual snails, slowed the feeding rate of P. canaliculata under the conditions of limited preferred species of decaying leaf litter. The decaying leaf litter of A. ilicifolius and S. apetala was the preferred food of P. canaliculata. As these snails have specific feeding preferences in mangrove forests, we speculated that P. canaliculata might have a nutritional niche overlap with native benthic snails in local habitats containing A. ilicifolius and (or) S. apetala when food sources are limited.

4.3. Relationship between Feeding Patterns and Characteristics of the Decaying Litter

P. canaliculata preferred the types of decaying leaf litter rich in nitrogen, phosphorous, protein, and ash. Nitrogen demand is common among benthic animals in mangrove forests. P. canaliculata preferred mangrove leaves with high nitrogen contents [25]. Our results indicated that P. canaliculata juveniles had a similar demand for nitrogen in decaying leaf litter in mangrove forests. The decomposition rate of litter was found to be affected by the high phosphorous content of mangrove leaves [61]. As for the phosphorous content, the feeding behavior of P. canaliculata is possibly different from that of the native mangrove crab, as previous research reported that the predation preference of the crab Neosarmatium malabaricum was not related to the phosphorous content in mangrove tissues [62]. P. canaliculata showed a positive food selection preference for mangrove leaves [25]; thus, our finding of a similar preference for decaying leaf litter is not surprising.
We found that the fiber content in the decaying leaf litter was not correlated with the feeding indicators of P. canaliculata, whereas the lignin content negatively affected the feeding indicators. P. canaliculata can efficiently digest the fiber contained in decaying leaf litter. Previous research reported that P. canaliculata had a high cellulase activity and application value in enzyme engineering [63]. The cellulase activity of P. canaliculata (up to 1.5 μmol∙min−1∙mg−1) [64] was much higher than the reported maximum activity (approximately 0.9 μmol∙min−1∙mg−1) measured based on eight species of benthic gastropods, crabs, and bivalves in a mangrove forest in southern China [65]. P. canaliculata had enough cellulase to digest the residual cellulose in the decaying leaf litter of the tested mangroves.
The ash of mangrove leaves is a complex inorganic–organic mixture and always contains abundant minerals accumulated in the mineral uptake of mangroves [38,66]. The ash content was found to be positively correlated with the feeding indicators of P. canaliculata. P. canaliculata could acquire their necessary nutrients from the ash of the decaying leaf litter of the tested mangroves. As for the lignin content, more research on the lignin-decomposing ability of P. canaliculata is required. We speculated that P. canaliculata lacks enough digestive enzymes to handle the lignin in decaying leaf litter. Likewise, calcium was not correlated with the feeding indicators of P. canaliculata. Seawater generally contains high concentrations of calcium. This phenomenon differs from that observed in freshwater environments, where calcium generally influences the freshwater snail populations of pomacea sp. [67].
Tannins, phenols, and flavonoids are chemical defense substances in fresh mangrove leaves [68]. Previous research reported that phenolic substances were detrimental to the consumption of decaying leaves of three macrophyte species [69]. Although the antioxidant and bacteriostatic activities weakened as the litter began to decay on the floor of the mangrove forest, a negative correlation between these substances and the feeding indicators of P. canaliculata was still observed in the study, which further proved the sensitivity of the snails to these toxic substances.
The feeding indicators of P. canaliculata were affected by the three representative decaying leaf characteristics, and four clusters for decaying leaf litter were observed. Compared with a single feeding indicator, the analysis of multiple indicators can help us to better understand the potential diet of P. canaliculata. Based on RDA and PCA, the types of decaying leaf litter can be distinguished by P. canaliculata in the invaded habitat. The snails can establish a population in mangroves composed of A. ilicifolius and S. apetala. Mangroves composed of A. ilicifolius and (or) S. apetala provide food for P. canaliculata through the accumulation of decaying leaf litter on the floor of the mangrove. In other words, even though the decaying leaf litter of the main mangrove species was not favorable for P. canaliculata, when coexisting with A. ilicifolius and (or) S. apetala, this species of mangrove might be vulnerable to P. canaliculata. A recent survey reported that the total area of S. apetala was 3804.86 ha in China in 2020 [70]. S. apetala was also an exotic mangrove species in China. It was widely planted in coastal areas and is gaining widespread attention due to its ecological impact. We discovered, for the first time, that the decaying leaf litter of S. apetala is suitable as a nutrient source for P. canaliculata, suggesting a possible hitchhike type of invasion of the mangrove ecosystem.

5. Conclusions

The feeding behavior of P. canaliculata was closely related to the species and characteristics of decaying leaf litter in this study. We concluded the following: (1) The decaying leaf litter of A. ilicifolius and S. apetala in mangroves could support the growth of juvenile P. canaliculata. (2) The juvenile P. canaliculata showed a different feeding preference for the tested types of decaying leaf litter. (3) The feeding preference of juvenile P. canaliculata was closely related to the chemical properties of decaying mangrove litter. In summary, the feeding behavior of P. canaliculata could accelerate nutrient release from decaying leaf litter into the sediment and alter the food chain in mangrove forests. As a global, invasive species, P. canaliculata potentially compromises conservation efforts for mangrove forests by acting as an invasive benthic consumer. However, the global distribution of P. canaliculata is restricted by climate change and local environmental factors such as water quality, interspecific competition, and nonspecific enemies. These limiting factors may partly influence the diet of P. canaliculata in mangroves. More studies need to be conducted on the role of P. canaliculata in the food chain in relation to climate change or local environmental factors in mangrove ecosystems.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jmse11030672/s1, Supplementary Figure S1 Newly laid egg clusters (A) and hatched eggs clusters (B) of apple snails in a mangrove forest; Supplementary Figure S2: Principal component analysis between chemical characteristics of decaying leaf litter of five mangroves and feeding indicators of Pomacea canaliculata. Supplementary Figure S3: Linear regression of inorganic components of chemical characteristics of decaying leaf litter and feeding indicators of P. canaliculata; Supplementary Figure S4: Linear regression of organic components of chemical characteristics of decaying leaf litter and feeding indicators of P. canaliculata; Supplementary Table S1: Linear regression parameters of inorganic chemical characteristics of decaying leaf litter and feeding indicators of Pomacea canaliculata; Supplementary Table S2: Linear regression parameters of organic chemical characteristics of decaying leaf litter and feeding indicators of Pomacea canaliculata.

Author Contributions

Conceptualization, J.L. and B.Z.; Formal analysis, J.L., Z.C. and Y.L. (Yunhui Li); Investigation, J.L., Z.C., Y.L. (Yunhui Li), D.C. and Y.H.; Resources, Z.C., D.C., Y.H., Y.L. (Yuexin Liao) and J.G.; Supervision, B.Z.; Writing—original draft, J.L.; Writing—review and editing, B.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (32001237; 31770484; 31901229); Guangdong Natural Science Foundation (2019A1515110719); Foundation of Heyuan Branch, Guangdong Laboratory for Lingnan Modern Agriculture Project (DT20220013); Foundation of Institute of Environment and Plant Protection, CATAS (HZSKFKT202203); Science and Technology Program of Guangzhou (SL2022B03J01006).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available at https://figshare.com/s/d8c72719fcf5107b831b (accessed on 10 December 2022).

Acknowledgments

We would like to thank the undergraduates in department of environmental ecological engineering of Guangdong University of Education for the assistance of samplings in mangrove wetlands. We thank anonymous reviewers for their valuable comments on the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Jmse 11 00672 g001 550
Figure 1. Boxplot of survival ratio ((A), blue) and specific growth ratio ((B), red) of P. canaliculata on decaying leaf litter of five species of mangroves. Species with the same letter are not significantly different (Kruskal–Wallis with Dunn–Bonferroni or Tukey tests).
Figure 1. Boxplot of survival ratio ((A), blue) and specific growth ratio ((B), red) of P. canaliculata on decaying leaf litter of five species of mangroves. Species with the same letter are not significantly different (Kruskal–Wallis with Dunn–Bonferroni or Tukey tests).
Jmse 11 00672 g001
Jmse 11 00672 g002 550
Figure 2. Boxplot of weight-specific daily feeding rate (WDR, g g−1 d−1) of P. canaliculata on decaying leaf litter of five mangroves under the multiple-choice condition (A) and the no-choice condition (B). Mangrove species includes A. ilicifolius (Acanthus ilicifolius), S. apetala (Sonneratia apetala), A. corniculatum (Aegiceras corniculatum), A. aureum (Acrostichum aureum), and K. candel (Kandelia candel). Species with the same letter are not significantly different (ANOVAs with Tukey or Kruskal–Wallis with Dunn–Bonferroni).
Figure 2. Boxplot of weight-specific daily feeding rate (WDR, g g−1 d−1) of P. canaliculata on decaying leaf litter of five mangroves under the multiple-choice condition (A) and the no-choice condition (B). Mangrove species includes A. ilicifolius (Acanthus ilicifolius), S. apetala (Sonneratia apetala), A. corniculatum (Aegiceras corniculatum), A. aureum (Acrostichum aureum), and K. candel (Kandelia candel). Species with the same letter are not significantly different (ANOVAs with Tukey or Kruskal–Wallis with Dunn–Bonferroni).
Jmse 11 00672 g002
Jmse 11 00672 g003 550
Figure 3. Redundancy analyses (RDA) of the correlations between feeding indicators and chemical characteristics of decaying leaf litter of five species of mangroves. WDR (g g−1 d−1)—weight-specific daily feeding rate under the multiple-choice condition; WDRN (g g−1 d−1)—weight-specific daily feeding rate under the no-choice condition.
Figure 3. Redundancy analyses (RDA) of the correlations between feeding indicators and chemical characteristics of decaying leaf litter of five species of mangroves. WDR (g g−1 d−1)—weight-specific daily feeding rate under the multiple-choice condition; WDRN (g g−1 d−1)—weight-specific daily feeding rate under the no-choice condition.
Jmse 11 00672 g003
Table
Table 1. Measurement of chemical characteristics of decaying leaf litter.
Table 1. Measurement of chemical characteristics of decaying leaf litter.
CharacteristicsMeasurement Method
CarbonPotassium dichromate oxidation method [35]
PhosphorousAscorbic acid-antimony reduced phosphate colorimetric method [36]
CalciumEDTA titrimetric method [37]
Protein and nitrogen contentNational Standards of China (GB 5009.5-2016)
AshDry ash method [38]
Crude fiberNational Standards of China (GB/T 5009.10-2003)
LigninKlason method [39]
Tannin and phenolEDTA method [40]
FlavonoidEthanol extraction method [41]
Table
Table 2. Correlation of inorganic chemical characteristics of decaying leaf litter and feeding indicators of Pomacea canaliculata.
Table 2. Correlation of inorganic chemical characteristics of decaying leaf litter and feeding indicators of Pomacea canaliculata.
Indicator
(g g−1 d−1)		Carbon
(g kg−1)		Nitrogen
(g kg−1)		C/N RatioCalcium
(%)		Phosphate
(g kg−1)
WDR(multiple-choice)−0.2840.485 *−0.3960.1090.685 **
WDR(no-choice)−0.0440.345−0.2570.2750.544 *
Note: The symbols * and ** indicate significant value (p < 0.01 or 0.05). WDR—weight-specific daily feeding rate.
Table
Table 3. Correlation of organic chemical characteristics of decaying leaf litter and feeding indicators of Pomacea canaliculata.
Table 3. Correlation of organic chemical characteristics of decaying leaf litter and feeding indicators of Pomacea canaliculata.
Indicator
(g g−1 d−1)		Ash
(g kg−1)		Fiber
(g kg−1)		Flavonoid
(g kg−1)		Lignin
(g kg−1)		Protein
(g kg−1)		Tannin
(g kg−1)		Phenolic
(g kg−1)
WDR(multiple-choice)0.531 *−0.169−0.697 **−0.695 **0.485 *−0.606 **−0.552 *
WDR(no-choice)0.644 **−0.176−0.755 **−0.527 *0.345−0.474 *−0.425
Note: The symbols * and ** indicate significant value (p < 0.01 or 0.05). WDR—weight-specific daily feeding rate.
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MDPI and ACS Style

Liu, J.; Chen, Z.; Li, Y.; Chen, D.; He, Y.; Zhao, B.; Liao, Y.; Guo, J. Potential Detritivorous Diet of the Invasive Apple Snail (Pomacea canaliculata Lamarck, 1822) in Mangroves: The Relationship between Feeding Indicators and Chemical Characteristics of Decaying Leaf Litter. J. Mar. Sci. Eng. 2023, 11, 672. https://doi.org/10.3390/jmse11030672

AMA Style

Liu J, Chen Z, Li Y, Chen D, He Y, Zhao B, Liao Y, Guo J. Potential Detritivorous Diet of the Invasive Apple Snail (Pomacea canaliculata Lamarck, 1822) in Mangroves: The Relationship between Feeding Indicators and Chemical Characteristics of Decaying Leaf Litter. Journal of Marine Science and Engineering. 2023; 11(3):672. https://doi.org/10.3390/jmse11030672

Chicago/Turabian Style

Liu, Jinling, Zhihua Chen, Yunhui Li, Danying Chen, Yulin He, Benliang Zhao, Yuexin Liao, and Jing Guo. 2023. "Potential Detritivorous Diet of the Invasive Apple Snail (Pomacea canaliculata Lamarck, 1822) in Mangroves: The Relationship between Feeding Indicators and Chemical Characteristics of Decaying Leaf Litter" Journal of Marine Science and Engineering 11, no. 3: 672. https://doi.org/10.3390/jmse11030672

APA Style

Liu, J., Chen, Z., Li, Y., Chen, D., He, Y., Zhao, B., Liao, Y., & Guo, J. (2023). Potential Detritivorous Diet of the Invasive Apple Snail (Pomacea canaliculata Lamarck, 1822) in Mangroves: The Relationship between Feeding Indicators and Chemical Characteristics of Decaying Leaf Litter. Journal of Marine Science and Engineering, 11(3), 672. https://doi.org/10.3390/jmse11030672

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