Next Article in Journal
Diversity and Life-Cycle Analysis of Pacific Ocean Zooplankton by Videomicroscopy and DNA Barcoding: Gastropods
Next Article in Special Issue
Spatial Distribution of the Taxonomic Diversity of Phytoplankton and Bioindication of the Shallow Protected Lake Borovoe in the Burabay National Natural Park, Northern Kazakhstan
Previous Article in Journal
Spatial Differences in Zooplankton Community Structure between Two Fluvial Lakes in the Middle and Lower Reaches of the Yangtze River: Effects of Land Use Patterns and Physicochemical Factors
Previous Article in Special Issue
Waterbodies in the Floodplain of the Drava River Host Species-Rich Macrophyte Communities despite Elodea Invasions
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 14
Issue 11
10.3390/d14110911
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Aquatic Insects in Habitat-Forming Sponges: The Case of the Lower Mekong and Conservation Perspectives in a Global Context

by
Nisit Ruengsawang
1,
Narumon Sangpradub
2 and
Renata Manconi
3,*
1
Division of Biology, Faculty of Science and Technology, Rajamangala University of Technology Krungthep, Bangkok 10120, Thailand
2
Applied Taxonomic Research Center, Department of Biology, Faculty of Science, Khon Kaen University, Khon Kaen 40002, Thailand
3
Department of Veterinary Medicine, University of Sassari, 07100 Sassari, Italy
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(11), 911; https://doi.org/10.3390/d14110911
Submission received: 15 July 2022 / Revised: 3 October 2022 / Accepted: 11 October 2022 / Published: 27 October 2022
(This article belongs to the Special Issue Diversity of Inland Wetlands: Important Roles in Mitigation of Human Impacts)
Browse Figures
Review Reports Versions Notes

Abstract

:
Shallow water sponges settled on a raft along the Pong River (Lower Mekong Basin, Thailand) were investigated to highlight the taxonomic richness, composition, relative abundance and lifestyle of sponge-dwelling aquatic Insecta. The three-dimensional biogenic structures of the model sponges hosted 4 orders of Insecta, belonging to 10 families and 19 genera/species, able to strictly coexist at the level of the sponges in aquiferous canals and/or at the body surface, and/or dwelling in the extracellular matrix. On the basis of the identified 379 larvae and pupae, Trichoptera and Diptera were found to be the dominant inhabitants of Corvospongilla siamensis (Demospongiae: Spongillida), endemic to Southeast Asia. In the focused lotic ecosystem, dominated by soft bottoms, sponges play a functional role. Insecta use sponges as a substratum, nursery ground, food source, and shelter microhabitat, protecting them from predation and environmental aggression. Moreover, their feeding behavior indicates the insects’ adaptive traits to recycle sponge siliceous spicules as a source of exogenous material to strengthen the larval–pupal cases and the digestive system. The results of the Thai sponge model contribute to the inventory of global engineering species richness, ecosystem types, and biogeographic diversity, thus raising awareness for freshwater biodiversity conservation. In this regard, the present data, along with the worldwide inventory, focus on sponges as (a) key habitat-forming species for aquatic insect assemblages, (b) ecosystem engineers in river/lake/wetland ecosystems, providing water purification, the processing of organic matter, recycling of nutrients, and freshwater–terrestrial coupling, and (c) promising candidates in restoration projects of tropical freshwater ecosystems by bioremediation.

1. Introduction

Spongillida (Demospongiae) inhabit and settle on a wide array of natural and artificial substrata in lotic and lentic water and wetlands in all continents, except Antarctica [1,2,3]. In the food web of freshwater ecosystems, sponges play a functional role as filter feeders, consuming the pelagic resources linking the pelagic and benthic trophic webs [4]. A sponge can filter up to 35 mL min−1(cm sponge)−3 [5]. This water volume is related to the sponge volume, oscule diameter, and water pumping rates, and could be affected by the temperature, food concentration, suspended sediment concentration, water flow, and viscosity [6,7,8]. This behavior was highlighted also in stressed conditions of sponge microcosms living in water rich with organic and bacterial loads in polluted sites during in situ experimental sponge aquaculture [9].
During their long-lasting lifecycle, continental sponges’ growth forms range from encrusting to massive and arborescent in the sessile adult phase, with a body size from a few millimeters to more than 1 m in diameter [1,2,10].
It is well known that the Spongillida (families Lubomirskiidae, Metaniidae, Potamolepidae, and Spongillidae) are associated with a diversified entomofauna worldwide, i.e., Ephemeroptera, Plecoptera, Odonata, Hemiptera, Megaloptera, Neuroptera, Trichoptera, Lepidoptera, Coleoptera, and Diptera, plus several other phyla ranging from bacteria to fishes and amphibians [1,2,11,12,13]. However, little is known about the diversity of sponge-dwelling aquatic insects and their relationship in Southeast Asia [14].
Investigations were carried out in the Lower Mekong Basin (Thailand, Oriental–Himalayan Region) to study (a) the composition, relative abundance, and taxonomic richness of sponge-dwelling aquatic insects, (b) their behavioral and ecological relationship, and (c) their biogeographic diversity. The data of insect–sponge associations are discussed also in comparison with the global dataset to highlight the sponges’ ecosystem services and to raise awareness of the biodiversity conservation of these peculiar living freshwater habitats.

2. Materials and Methods

2.1. Study Area

This study was carried out in the Pong River (16°46’19.9´´ N, 102°38´3.25´´ E) which is a tributary of the Lower Mekong Basin (Figure 1) by the largest hydrographic basin of Northeastern Thailand. This regulated river provides an important water resource for agriculture, domestic uses, aquaculture, recreation, electricity generation, and industrial purposes, especially in Khon Kaen Province. Water is released from the outlet of the Ubolratana Dam to the lower part of the Pong River for water management, such as supplying water for agriculture and preventing water degradation by the operation of the Electricity Generating Authority Thailand, both in the wet (June–November) and dry (December–May) seasons. This eutrophic river, dominated by silty bottoms and having the most altered water quality of this region, since 1993, has been polluted from multiple sources, e.g., agricultural run-off, a pulp and paper mill, and a fertilizer factory [15,16]. Nevertheless, the water quality was in a generally fair condition, according to the surface water quality standard and water quality index [17].
The study site, Ban Huai Sai, is located at 165 m asl (16°46′19.9″ N, 102°38′3.25″ E) ~1.5 km downstream from the outlet of the Ubolratana Dam (Figure 2). The riverbed is characterized by a maximum depth of 8 m and width of 70 m. The submerged substrata range from silty bottoms, timbers, and aquatic plants to artificial manufacture along the banks, e.g., fish cage nets, submerged structures of rafts, and nylon lines. The riparian vegetation mainly consists of the rain tree, Samanea saman (Jacq.) Merr. The aquatic vegetation mainly consists of Colocasia sp., Hydrilla verticillata (L. f.) Royle, Cyperus sp., and Nephrolepis sp. Sponges of the order Spongillida (Demospongiae) were found on the twigs and the bottom of the riverbed [19]. Flourishing and abundant sponge populations were also settled on the submerged artificial substrata, floating raft construction, buoys, and recreational fishing nylon lines trapped in the raft buoys at the study site (Figure 2a).

2.2. Sampling Methods

Fourteen specimens of sponges were collected in February 2008 (dry season, northeast monsoon) at two water depths, i.e., 0.3 m from the submerged raft construction (seven sponges), and 1 m on the nylon lines (seven sponges) (Figure 2b). These specimens were ascribed to Corvospongilla siamensis, Manconi & Ruengsawang, 2012. The identification of the sponges was based on the growth form, skeletal architecture, and microtraits. Detailed analyses of the gemmular theca and its gemmuloscleres, together with the skeletal microscleres and megascleres, were carried out [20,21,22]. All the sponges considered in the study were covered with a hand net of 450 µm mesh size, carefully detached from the substrate, and then placed into plastic bags. To allow most of the aquatic insects to leave their hosts, each sample with its river water was placed in a plastic tray for half an hour (ambient temperature), and then it was preserved in 70% ethanol. Each sponge was photographed in the field. In the laboratory, the samples were washed through a 500 µm mesh-size sieve, and the associated insects remaining on the surface of the sponges and sieve were collected by forceps. Each sponge was also carefully dissected to collect the insects that remained within its body. All the aquatic insects were sorted, identified to the lowest possible taxonomic level, and counted by screening at the microscope. The taxonomic identification of the insects from Ban Huai Sai was based on Morse et al. [23], Epler [24], Sangpradub and Boonsoong [25], and Cranston [26]. The similarities in the aquatic insect composition between the screened sponge specimens were analyzed by cluster analysis, using Jaccard’s similarity index, by PC-ORD software version 5.10.
The gut contents of the dominant insect taxa were investigated qualitatively by light microscopy for their primary dietary components. Thirty specimens of each taxon were dissected under a stereomicroscope; their digestive tracts were mounted on slides and examined under a compound microscope. The cases of the trichopterans (n = 15) and tubes of the chironomids (n = 15) were examined and photographed by a scanning electron microscope (SEM, LEO model 1450VP) to determine whether these insects use the sponge spicules to construct their cases or tubes.
The water quality parameters were evaluated at two shallow water depths, (0.3 m and 1 m), during the dry season–northeast monsoon. The water quality parameters, such as dissolved oxygen (DO), electrical conductivity, total dissolved solids (TDS), water temperature, pH and flow velocity, were measured in the field, along with the collections of sponges at each depth, by portable digital instruments (a dissolved oxygen meter YSI model 57 (Yellow Spring Instrument Co. Inc., Yellow Spring, MP, USA); conductivity meter Fisher Scientific model 09-326-2 (Fisher Scientific International Inc., Pittsburgh, PA, USA); pH meter HACH sensionTM1 (HACH Company, Loveland, CO, USA); Genuine Gurley® current meter model D625 digital pygmy meter with Model 1100 Flow Velocity Indicator (Gurley Precision Instruments, New York, NY, USA)). The suspended solids (SS), turbidity, nitrate, and phosphate were measured in the laboratory by the HACH DR/2010 Spectrophotometer (HACH Company, Loveland, CO, USA). The biological oxygen demand (5 days, 20 °C) (BOD5) was also evaluated. The difference in the environmental parameters between the two water depths was determined by the Mann–Whitney U test with SPSS for Windows software, version 16.

3. Results

3.1. Physicochemical Parameters

The mean values of most of the physicochemical parameters were not significantly different between 0.3 m and 1 m, except flow velocity and DO, which were significantly higher at 1.0 m (p < 0.05, Supplementary Materials Table S1). Due to unavailable data from the deep zone, the comparative analyses on the suspended solids, turbidity, nitrate, and phosphate at the different water depths were not carried out.

3.2. Composition and Abundance of Associated Aquatic Insects

A total of 379 larvae and pupae of aquatic insects belonging to 4 orders, 10 families, and 19 taxa were recorded, by microscopical screening, from 14 sponge samples at two water depths at Ban Huai Sai (Table 1; Figure 3, Figure 4, Figure 5 and Figure 6). The dominant larvae colonizing C. siamensis were Trichoptera (48.81%) and Diptera (47.75%) (Figure 3b–d), whereas Neuroptera and Ephemeroptera were less represented. The relative abundance of associated insect taxa varied from 3 to 94 individuals per sponge specimen and ranged from 140 specimens (14 taxa) at 0.3 m depth to 239 specimens (16 taxa) at 1 m depth. The egg jelly envelops of Povilla heardi Hubbard, 1984 (Ephemeroptera, Polymitarcyidae) were also found on the sponge surface (Figure 6a,b).
The most dominant taxa in the Pong River were Ecnomus spp., followed by Amphipsyche meridiana Ulmer, 1909 (Trichoptera), Polypedilum sp., and Xenochironomus sp. (Diptera), making up 77.8% of the specimens. The larval stages of first three genera are clingers, but Xenochironomus is a burrower in sponges. Eleven taxa were shared by both water depths, i.e., Polypedilum sp. was present in all the samples, followed by Ecnomus and Xenochironomus, respectively. The chironomid larvae Ablabesmyia and Dicrotendipes were found from six out of the seven sponges at the 0.3 m water depth. The larvae of Sisyra sp. were only 2.3% (n = 9), the pupae of chironomids 2.3% (n = 9), and the caddisflies 1% (n = 4) were also recorded (Table 1). The cluster analysis, based on Jaccard’s similarity index, relying on presence/absence data, showed differences in the aquatic insect composition among the fourteen sponge samples and separated them into two main clusters (Figure 7). One cluster comprised the shallow-water samples (0.3 m) and the other comprised all but one of those from the deep water (1 m).

3.3. Gut Content Analysis

The gut content analysis of the four dominant taxa, i.e., Ecnomus spp., A. meridiana, Polypedilum sp., and Xenochironomus sp., respectively, showed a predominance of detritus, followed by diatoms, fine detritus material, rotifers, and sponge siliceous spicules (Figure 8c,d). Generally, the entire strongyle megascleres characterized by rounded tips were commonly found in the digestive tract, whereas fragments of these spicules rarely occurred. The percentage of spicules occurring in the gut contents of the representative dominant genera showed a wide range, i.e., Ecnomus spp. (70%; Trichoptera), A. meridiana (56.6%; Trichoptera), Xenochironomus sp. (6.6%; Chironomidae), and Polypedilum sp. (6.6%; Chironomidae). In addition, megascleres and microscleres of sponges were also found in the chironomids Ablabesmyia sp. and Paramerina sp.
The texture of the pupal case of the A. meridiana studied by an SEM showed that silk thread is a major component of the case, strengthened by two types of sponge spicules (microscleres, gemmuloscleres, and megascleres) on both the inner and outer layers of the cases (Figure 5a,b). The observations on the tubes of the chironomid larvae and pupae stages highlighted that both are made, in part, by sponge spicules (Figure 5c,d).

4. Discussion

4.1. Freshwater Sponges as Microhabitat for Associated Insects

The data highlight that many insects can inhabit sponges in the Mekong River Basin (Table 1), matching the previous studies on sponge-dwelling entomofauna, reporting 10 orders of Insecta inhabiting almost 20 Spongillida species from all the biogeographic regions, except Antarctica (Table 2). The flourishing population of Corvospongilla (Figure 9) is a temporary microhabitat for the long-lasting larval and pupal stages of many insects, either at the body surface and canals, or within the extracellular matrix, suggesting that, also, other Spongillida species play the same functional role as the habitat-forming species in the same site, e.g., Oncosclera asiatica [28].

4.2. Associated Insects and Environmental Conditions

Even though the dissolved oxygen (DO) was significantly different between the two depths, it did not seem to affect the sponge-dwelling insect assemblage structure, i.e., the relative abundance and taxonomic richness.
The flow-velocity data also support the fact that the DO is not a limiting factor to the sponges’ inhabitants in the study site, which is located near the outlet of the dam. This could be due to both the oxygen contribution from the sponge algal symbiont (endocellular) and the hydrodynamic condition of the sponge microenvironment. Indeed, the sponges’ pumping activity, involving conspicuous amounts of water, creates a microcirculation, both within the sponge body (inner canals and cavities) and at its irregular surface (inhalant openings with incurrent and oscules with outcurrent water), matching the previous data [87,88].
Although the composition of the associated aquatic insects between the shallow and deep zones is similar in sharing 11 taxa, it seems that the flow-velocity values could be a factor that affects the number of Amphipsyche meridiana, inhabiting only two samples in the deeper zone, while the higher values may favor these net-spinning larvae. In addition, the division between the “shallow and deeper parts” of the cluster differs in the greater abundance of Trichoptera, from the genus Ecnomus and Amphipsyche, requiring higher oxygen concentrations than the chironomids, which is also confirmed by the environmental data and could be the consequence of the higher flow velocity.
The colonization of Polypedilum sp. in all the samples indicates that Corvospongilla is a favorable habitat matching the known wide habitat range of this chironomid genus [24,69]. The present data, reporting Chironomidae larvae fairly commonly in the sponges from both the two shallow zones, match those of the Chironomidae [48,61,69], which is well represented in the Pong River’s soft bottom, ranging from pristine to impacted water quality conditions [89]. Further in-depth analyses of the taxonomy and diversity of the chironomid larvae in the Pong River will be essential to clarify the sponge–midge interactions.
The present data also corroborate those of Gugel [45], who reported that the high larvae number of Ecnomus tenellus (Rambur, 1842) and Hydropsyche sp. occurring on European sponges was higher than their occurrence independently from sponges. The results confirm that sponges represent a favorable habitat for these larvae, as reported also by Annandale [29,90] for other hydrographic basins of the Asian tropics.

4.3. Aquatic Insect Abundance, Sponge Size and Body Architecture

The high number of sponge-dwelling aquatic insects in this study occurred in a silty riverbed with a dense population of long-living, massive sponges, characterized by a 3D body architecture, rich in large inner canals/cavities and exhalant apertures (Figure 3a, Figure 4a,b and Figure 9), matching the investigations on marine sponge canals diameter and body morphology inhabited by invertebrates [91,92]. The sponge body architecture, rich in cavities, seems to provide a suitable space for some aquatic insects to segregate and avoid predators, as suggested also by the high density of freshwater African A. meridiana in vesicular rocks (i.e., volcanic rock pitted with many cavities/vesicles at its surface and inside), which was about 10 times higher than those of non-vesicular rocks [93].
Only the biomass and numbers of three species of amphipods inhabiting sponges are known to be correlated with the weight of a Baikalian sponge species, according to Kamaltynov et al. [43], but the other fauna including insects showed no correlation.

4.4. Interspecific Relationships between Aquatic Insects and Sponges

Several genera of Insecta have been recognized as obligatory associated with sponges, i.e., Ceraclea (Trichoptera), Demeijerea, Oukuriella, Xenochironomus (Chironomidae), Climacea, and Sisyra (Neuroptera) [46,47,53,54,60,69,72,76,82,94] (see Table 2). Spongivory is, however, rare, probably due to the production of sponge toxins and repellents [13,95]. Sisyridae larvae are well known as obligate predators (spongivory) of freshwater sponges [71,76,84,96].
In the present study, the type of sponge–insect relationship ranges from incidental to obligate. The larvae of Sisyra and Xenochironomus we discovered in sponges had never been found in the Pong River’s macroinvertebrate community [89,97,98]. Weissmair and Warninger [99] stated that the Sisyra adults need rich riparian habitats, which occur rarely along the Pong River. This datum reinforces the opinion that the larvae of these taxa are strictly associated with freshwater sponges.
Little information has been published in Asia on the Sisyra biology, ecology, and phylogeny [100,101]. Only two species, Sisyra indica Needham, 1909, and Sisyra maculata Monserrat, 1981, are known from Thailand [83,84,102,103], suggesting further studies on neglected neuropterans and Xenochironomus species and their life cycles in tropical sponges of Asia would be worthwhile.

4.5. Sponges and Gut Content of Their Associated Aquatic Insects

Roback [72] reported that the digestive tracts of caddisfly larvae belonging to the genus Athripsodes were filled with debris and sponge spicules. These larvae ingest the sponge tissues and do not merely use them as an occasional substrate or case-building material. In this study, the gut contents of the caddisfly A. meridiana larvae (Figure 8a–d), showing high percentages of diatoms, may indicate that these net-spinning caddisfly larvae are filtering collectors. Our results agree with Boon [104], who concluded that the well-developed gastric mill plates of A. meridiana are ideal for crushing diatoms. Although it is known that sponges are not edible for most animals, due to their chemical deterrence, with hard skeletal components and bioactive compounds, the occurrence of many spicules in the digestive tracts may also suggest that A. meridiana feeds on the tissues of the sponge when moving on its surface, which matches the previous reports [47,72]. Entire siliceous strongyle spicules in the digestive tract could improve the grinding or filtering of foods, as suggested by not breaking down—even passing—the proventriculus, which consists of large tooth plates ranging from 533 to 656 μm in length (Figure 8c). Moreover, it seems that the spicules of C. siamensis, with typical blunt tips, cannot create a risk of damage to the gut wall of spongivor insects, contrasting with the condition of caddisfly Ceraclea fulva (Rambur, 1842), displaying an abnormally thick peritrophic membrane shielding its soft internal tissues from ingested spicules, with acute tips, of the sponge Ephydatia fluviatilis [46,47].
As for the pupal case of A. meridiana, an SEM analysis showed that sponge spicules were interwoven in the case wall, which is similar to those observed in C. fulva. So, these spicules seem to be useful material to reinforce the cases of the caddisfly larvae (Figure 5a,b). The chironomid larvae and pupae also utilized the sponge spicules for constructing their tubes and cases in the Pong River (Figure 5c,d), thus corroborating previous data on the occurrence of sponge spicules in the gut [94].

4.6. Biodiversity and Conservation Perspectives

The results of this study expand our knowledge of freshwater sponges in Southeast Asia, which is considered a biodiversity hotspot, highlighted by the 3007 new species of vascular plants, fishes, amphibians, reptiles, birds, and mammals discovered in the Greater Mekong region between 2007 and 2020 [105,106]. The description of three new Spongillida species and a new record in Thailand and Vietnam [20,28,107,108], and ongoing discoveries in Thailand (Ruengsawang unpublished data), indicate that the sponges inhabiting rivers, lakes, and wetlands in this region remain unexplored and are underestimated in their biodiversity. Environmental impacts on freshwater sponges have been reported, i.e., temperature, heavy metal contamination [109], and habitat change, as one of biodiversity loss drivers in Southeast Asia [110]. Therefore, a diversity assessment of this neglected fauna is urgently needed.
In the case of the Pong River, the biofouling by sponges in fish culture, resulting in clogging of the nets and decreased water circulation, was frequently found in the previous and current studies [19]. Fish farmers lift their cage nets from the water to dry and remove sponges for maintenance after fish harvesting (Figure 9 and Figure 10). Skin irritation caused by sponge spicules was also reported by the farmers. The advantages and disadvantages of sponges biofouling in the fish culture in the Pong River need further research to fully understand to demonstrate the ecological value of these animals.
From the conservation aspect, it is clear that freshwater sponges play an important role in aquatic ecosystems as biofilters, through their filter-feeding and water-pumping activities and are vulnerable habitats for aquatic insects. The opportunistic insect from this study, A. meridiana, adopts a variety of strategies to colonize and to use sponges as a microhabitat, which agrees with Boon [93]. Despite freshwater sponges not being threatened globally [1,10,109,111], the conservation and monitoring of freshwater sponges in tropical Asia are needed to understand their status.

Synthesis

The data indicate that, worldwide, freshwater sponges perform functional roles as ecosystem engineers, sensu Jones et al. [112]. They supply to insects: (a) persistent heterogeneous substrata and microclimatic conditions related to the sponges’ massive to arborescent growth form and their physiological performance, (b) ecological refugia and breeding/nursery grounds as a sheltering microhabitat for settling and the development of eggs, (c) food source for detritivores by the continuous water-flow, trapping particulate organic matter, as a foraging area, for eating on sponge-associated algae, and as prey for predatory species on other hosted insects and a plethora of other invertebrates, (d) the morpho-functional role of the siliceous spicules to strengthen the larval insect’s digestive system and the cases of larvae and pupae, (e) protection against predators, (f) shelter for withstanding floods, high siltation, and desiccation (dry season) during water level fluctuations. Despite the sponges’ functional role as biofilters, on occasion, local people consider these animals responsible for economic damage, e.g., on the health of fish in farming cages along the Lower Mekong River. In agreement with the restoration science proposed by Ormerod [113], we suggest that sponge farming in inland water could be an effective nature-based solution to reduce biodiversity loss, as a management tool, by enhancing the water quality. This is particularly relevant in tropical freshwater to support bioremediation projects in restoring the environmental value, also in giving economic benefits to the local people. Another key point could be a targeted action on the people’s environmental education in order to raise awareness of freshwater bioresources conservation.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d14110911/s1; Table S1: Mean values (±SD) for physicochemical parameters during the dry season (northeast monsoon) at two shallow water depths inhabited by a flourishing population of Corvospongilla siamensis and its associated insects in the Pong River (Lower Mekong, Thailand).

Author Contributions

All authors contributed equally to the conceptualization, methodology, validation, formal analysis, investigation, resources, data curation, writing—original draft preparation, writing—review and editing, visualization, supervision, project administration, and funding acquisition. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Thailand Research Fund (TRF), in collaboration with the Commission on Higher Education, under grant number MRG6080200, the Office of the Higher Education Commission, Thailand, under the program “Strategic Scholarships for Frontier Research Network“ for the Joint Ph.D. Program Thai Doctoral degree. Funding to R. Manconi was provided by the Università di Sassari [grant Fondo di Ateneo per la Ricerca 2019-2021], Fondazione di Sardegna [grant FdS/RAS-2016/CUP J86C1800082005], Regione Autonoma della Sardegna [grant RAS2012-LR7/2007-CRP-60215], and Parco Nazionale dell’Asinara [grant PNA-2016].

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We would like to thank Roberto Pronzato and Martin Spies for their valuable comments. We thank also Boonsong Kongsook (Applied Taxonomic Research Center, Division of Biology, Faculty of Science, Khon Kaen University) for the SEM assistance. Special thanks go to Chawalit Wongsanorasaet for the study site data and Paiboon Getwongsa for the field assistance.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Manconi, R.; Pronzato, R. Global Diversity of Sponges (Porifera: Spongillina) in Freshwater. Hydrobiologia 2008, 595, 27–33. [Google Scholar] [CrossRef]
  2. Manconi, R.; Pronzato, R. Chapter 8—Phylum Porifera. In Thorp and Covich’s Freshwater Invertebrates, 4th ed.; Thorp, J.H., Rogers, D.C., Eds.; Academic Press: Boston, MA, USA, 2015; pp. 133–157. ISBN 978-0-12-385026-3. [Google Scholar]
  3. Manconi, R.; Pronzato, R. Chapter 3—Phylum Porifera. In Thorp and Covich’s Freshwater Invertebrates, 4th ed.; Thorp, J.H., Rogers, D.C., Eds.; Academic Press: Boston, MA, USA, 2016; pp. 39–83. ISBN 978-0-12-385028-7. [Google Scholar]
  4. Skelton, J.; Strand, M. Trophic Ecology of a Freshwater Sponge (Spongilla Lacustris) Revealed by Stable Isotope Analysis. Hydrobiologia 2013, 709, 227–235. [Google Scholar] [CrossRef]
  5. Weisz, J.B.; Lindquist, N.; Martens, C.S. Do Associated Microbial Abundances Impact Marine Demosponge Pumping Rates and Tissue Densities? Oecologia 2008, 155, 367–376. [Google Scholar] [CrossRef]
  6. Reiswig, H.M. Particle Feeding in Natural Populations of Three Marine Demosponges. Biol. Bull. 1971, 141, 568–591. [Google Scholar] [CrossRef]
  7. Morganti, T.M.; Ribes, M.; Yahel, G.; Coma, R. Size Is the Major Determinant of Pumping Rates in Marine Sponges. Front. Physiol. 2019, 10, 1474. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  8. Morganti, T.M.; Ribes, M.; Moskovich, R.; Weisz, J.B.; Yahel, G.; Coma, R. In Situ Pumping Rate of 20 Marine Demosponges Is a Function of Osculum Area. Front. Mar. Sci. 2021, 8, 583188. [Google Scholar] [CrossRef]
  9. Ledda, F.D.; Pronzato, R.; Manconi, R. Mariculture for Bacterial and Organic Waste Removal: A Field Study of Sponge Filtering Activity in Experimental Farming. Aquac. Res. 2014, 45, 1389–1401. [Google Scholar] [CrossRef]
  10. Manconi, R.; Pronzato, R. How to Survive and Persist in Temporary Freshwater? Adaptive Traits of Sponges (Porifera: Spongillida): A Review. Hydrobiologia 2016, 782, 11–22. [Google Scholar] [CrossRef]
  11. Frost, T.M.; Reiswig, H.M.; Ricciardi, A. Porifera. In Ecology and Classification of North American Freshwater Invertebrates; Thorp, J.H., Covich, A.P., Eds.; Academic Press: New York, NY, USA, 2001; pp. 97–133. [Google Scholar]
  12. Pronzato, R.; Manconi, R. Atlas of European Freshwater Sponges. Ann. Mus. Civ. Storia Nat. Ferrara 2001, 4, 3–64. [Google Scholar]
  13. Reiswig, H.M.; Frost, T.M.; Ricciardi, A. Porifera. In Ecology and Classification of North American Freshwater Invertebrates, 3rd ed.; Thorp, J.H., Covich, A.P., Eds.; Academic Press: London, UK, 2010; pp. 91–123. [Google Scholar]
  14. Manconi, R.; Ruengsawang, N.; Vannachak, V.; Hanjavanit, C.; Sangpradub, N.; Pronzato, R. Biodiversity in South East Asia: An Overview of Freshwater Sponges (Porifera: Demospongiae: Spongillina). J. Limnol. 2013, 72, e15. [Google Scholar] [CrossRef] [Green Version]
  15. Mizuno, T.; Mori, S. Preliminary Hydrobiological Survey of Some Southeast Asian Inland Waters. Biol. J. Linn. Soc. 1970, 2, 77–118. [Google Scholar] [CrossRef]
  16. Sangsurasak, C.; Hsieh, H.-N.; Wongphathanakul, W.; Wirojanagud, W. Water Quality Modeling in the Nam Pong River, Northeast Thailand. ScienceAsia 2006, 32, 071. [Google Scholar] [CrossRef]
  17. Pollution Control Department. Thailand State of Pollution Report 2007; Pollution Control Department: Bangkok, Thailand, 2007. [Google Scholar]
  18. Van Zalinge, N.; Degen, P.; Pongsri, C.; Nuov, S.; Jensen, J.G.; Nguyen, V.H.; Choulamany, X. The MekongRiverSystem; RAP publication 16; FAO Regional Office for Asia and the Pacific: Phnom Penh, Cambodia, 2004. [Google Scholar]
  19. Ruengsawang, N. The Distribution, Growth, Reproduction, and Ecology of Freshwater Sponges in the Pong River. Ph.D. Dissertation, Khon Kaen University, Khon Kaen, Thailand, 2013. [Google Scholar]
  20. Ruengsawang, N.; Sangpradub, N.; Hanjavanit, C.; Manconi, R. Biodiversity Assessment of the Lower Mekong Basin: A New Species of Corvospongilla (Porifera: Spongillina: Spongillidae) from Thailand. Zootaxa 2012, 3320, 47–55. [Google Scholar] [CrossRef]
  21. Manconi, R.; Erpenbeck, D.; Fromont, J.; Wörheide, G.; Pronzato, R. Discovery of the Freshwater Sponge Genus Corvospongilla Annandale (Porifera: Spongillida) in Australia with the Description of a New Species and Phylogeographic Implications. Limnology 2022, 23, 73–87. [Google Scholar] [CrossRef]
  22. Manconi, R.; Pronzato, R. The Genus Corvospongilla Annandale, 1911 (Porifera: Demospongiae: Spongillida) from Madagascar Freshwater with Description of a New Species: Biogeographic and Evolutionary Aspects. Zootaxa 2019, 4612, 544–554. [Google Scholar] [CrossRef] [PubMed]
  23. Morse, J.C.; Yang, L.; Tian, L. Aquatic Insects of China Useful for Monitoring Water Quality, 1st ed.; Hohai University Press: Nanjing, China, 1994. [Google Scholar]
  24. Epler, J.H. Identification Manual for the Larval Chironomidae (Diptera) of North and South Carolina; North Carolina Department of Environment and Natural Resources: Raleigh, NC, USA, 2001. [Google Scholar]
  25. Sangpradub, N.; Boonsoong, B. Identification of Freshwater Invertebrates of the Mekong River and Its Tributaries; Mekong River Commission: Vientiane, Laos, 2006; ISBN 978-92-95061-00-2. [Google Scholar]
  26. Cranston, P.S. The Chironomidae Larvae Associated with the Tsunami-impacted Waterbodies of the Coastal Plain of Southwestern Thailand. Raffles Bull. Zoo. 2007, 55, 231–244. [Google Scholar]
  27. Sangpradub, N.; Giller, P.S. Gut Morphology, Feeding Rate and Gut Clearance in Five Species of Caddis Larvae. Hydrobiologia 1994, 287, 215–223. [Google Scholar] [CrossRef]
  28. Manconi, R.; Ruengsawang, N.; Ledda, F.D.; Hanjavanit, C.; Sangpradub, N. Biodiversity Assessment in the Lower Mekong Basin: First Record of the Genus Oncosclera (Porifera: Spongillina: Potamolepidae) from the Oriental Region. Zootaxa 2012, 3544, 41–51. [Google Scholar] [CrossRef]
  29. Annandale, N. Notes on the freshwater fauna of India. No. 5. Some animals found with Spongilla carteri in Calcutta. J. Asiat. Soc. Bengal 1906, 2, 187–196. [Google Scholar]
  30. Schröder, K. Spongillidenstudien VII, Susswasserschwamme von Neuseeland, Borneo und Madagaskar. Zool. Anz. 1935, 109, 97–106. [Google Scholar]
  31. Mansell, M.W. Neuropterology in Southern Africa. In Recent Research in Neuropterology: Proceedings of the 2nd International Symposium on Neuropterology (Insecta, Megaloptera, Raphidioptera, Planipennia), Hamburg, Germany, 20–26 August 1984; Gepp, J., Aspock, H., Hölzel, H., Eds.; Gedruckt von Druckhaus Thalerhof: Österreich, Austria, 1986; pp. 45–52. [Google Scholar]
  32. Wells, A. New Caledonian Hydroptilidae (Trichoptera), with New Records, Descriptions of Larvae and a New Species. Aquat. Insects 1995, 17, 223–239. [Google Scholar] [CrossRef]
  33. Wells, A.; Johanson, K. Review of the New Caledonian Species of Acritoptila Wells, 1982 (Trichoptera, Insecta), with Descriptions of 3 New Species. ZooKeys 2014, 397, 1–23. [Google Scholar] [CrossRef] [Green Version]
  34. Forteath, G.N.R.; Osborn, A.W. Biology, Ecology and Voltinism of the Australian Spongillafly Sisyra Pedderensis Smithers (Neuroptera: Sisyridae). Pap. Proc. R. Soc. Tasman. 2012, 146, 25–35. [Google Scholar] [CrossRef] [Green Version]
  35. Forteath, G.N.R.; Purser, J.; Osborn, A.W. A New Species of Sisyra Burmeister 1839 (Neuroptera: Sisyridae) from Four Springs Lake and Wadley’s Dam, Northern Tasmania. Austral Entomol. 2015, 54, 217–220. [Google Scholar] [CrossRef]
  36. Pavesi, P. Di una spugna d’acqua dolce nuova per l’Italia. Rendiconti del Reale Istituto Lombardo di Scienze e Lettere Ser. II 1881, 14, 1–6. [Google Scholar]
  37. Arndt, W. Porifera, Schwämme, Spongien. In Die Tierwelt Deutschlands und der Angrenzenden Meeresteile nach ihren Merkmalen und ihrer Lebensweise 4 (Porifera-Hydrozoa-Coelenterata-Echinodermata); Dahl, F., Ed.; Gustav Fischer Verlag: Leipzig, Germany, 1928; pp. 1–94. [Google Scholar]
  38. Rezvoi, P.D. Presnovodnye gubki. [Freshwater sponges]. In Fauna SSSR [The Fauna of the USSR]; Rezvoi, P.D., Ed.; Akad Nauk SSSR: Moscow, Russia, 1936; Volume 2. (In Russian) [Google Scholar]
  39. Berg, K. Biological studies on the river Susaa. Faunistic and biological investigations. Porifera. Folia Limnol. Scand. 1948, 4, 10–23. [Google Scholar]
  40. Gaumont, J. L’appareil digestif de la larve d’un Planipenne associé aux éponges d’eau douce: Sisyra fuscata. Ann. Soc. Entomol. Fr. (NS) 1965, 1, 335–357. [Google Scholar]
  41. Moretti, G.; Corallini-Sorcetti, C. Al Lago Trasimeno è arrivata Ceraclea fulva Ramb. (Trichoptera–Leptoceratidae). Riv. Idrobiol. 1980, 19, 1–9. [Google Scholar]
  42. Konopacka, A.; Siciński, J. Macrofauna Inhabiting the Colonies of the Sponge Spongilla lacustris (L.) in the River Gać. SIL Proc. 1922–2010 1985, 22, 2968–2973. [Google Scholar] [CrossRef]
  43. Kamaltynov, R.M.; Chernykh, V.I.; Slugina, Z.V.; Karabanov, E.B. The Consortium of the Sponge Lubomirskia Baicalensis in Lake Baikal, East Siberia. Hydrobiologia 1993, 271, 179–189. [Google Scholar] [CrossRef]
  44. Weissmair, V.W.; Mildner, P. Zur Kenntnis der Schwammfliegen (Neuroptera: Sisyridae), ihrer Wirte und Wohngewässer in Kärnten. Carinthia II 1995, 105(2), 535–552. [Google Scholar]
  45. Gugel, J. Life Cycles and Ecological Interactions of Freshwater Sponges (Porifera, Spongillidae) in the River Rhine in Germany. Limnologica 2001, 31, 185–198. [Google Scholar] [CrossRef] [Green Version]
  46. Corallini, C.; Gaino, E. Peculiar Digestion Patterns of Sponge-Associated Zoochlorellae in the Caddisfly Ceraclea Fulva. Tissue Cell 2001, 33, 402–407. [Google Scholar] [CrossRef] [PubMed]
  47. Corallini, C.; Gaino, E. The Caddisfly Ceraclea fulva and the Freshwater Sponge Ephydatia Fluviatilis: A Successful Relationship. Tissue Cell 2003, 35, 1–7. [Google Scholar] [CrossRef]
  48. Gaino, E.; Lancioni, T.; La Porta, G.; Todini, B. The Consortium of the Sponge Ephydatia fluviatilis (L.) Living on the Common Reed Phragmites Australis in Lake Piediluco (Central Italy). Hydrobiologia 2004, 520, 165–178. [Google Scholar] [CrossRef]
  49. Wallace, I.D.; Wallace, B.; Philipson, G.N. Keys to the Case-Bearing Caddis Larvae of Britain and Ireland; Freshwater Biological Association—Scientific Publication: Ambleside, UK, 2003; Volume 61, p. 259. [Google Scholar]
  50. Weinberg, I.; Glyzina, O.; Weinberg, E.; Kravtsova, L.; Rozhkova, N.; Sheveleva, N.; Natyaganova, A.; Bonse, D.; Janussen, D. Types of interactions in consortia of Baikalian sponges. Boll. Mus. Ist. Biol. Univ. Genova 2004, 68, 655–663. [Google Scholar]
  51. Loru, L.; Pantaleoni, R.A.; Sassu, A. Overwintering Stages of Sisyra iridipennis A. Costa, 1884 (Neuroptera Sisyridae). Ann. Mus. Cívico Stor. Nat. Ferrara 2007, 8, 153–159. [Google Scholar]
  52. Schiffels, S. Commensal and parasitic Chironomidae. Lauterbornia 2009, 68, 9–33. [Google Scholar]
  53. Sokolova, A.M.; Palatov, D.M. Macroinvertebrate Associations of Sponges (Demospongiae: Spongillidae) from some Fresh Waters in the Palaearctic (in Russian). Povolzhskiy J. Ecol. 2014, 4, 618–627. [Google Scholar]
  54. Palatov, D.M.; Sokolova, A.M. Freshwater Sponges and Their Associated Invertebrates in the Great Lakes Basin (Mongolia). Ukr. J. Ecol. 2017, 7, 635–639. [Google Scholar] [CrossRef] [Green Version]
  55. Zvereva, Y.; Medvezhonkova, O.; Naumova, T.; Sheveleva, N.; Lukhnev, A.; Sorokovikova, E.; Evstigneeva, T.; Timoshkin, O. Variation of Sponge-Inhabiting Infauna with the State of Health of the Sponge Lubomirskia Baikalensis (Pallas, 1776) in Lake Baikal. Limnology 2019, 20, 267–277. [Google Scholar] [CrossRef]
  56. Ostrovsky, A.M. New Finds and Species of Caddisflies (Trichoptera) in Southeastern Belarus. Inland Water Biol. 2021, 14, 133–140. [Google Scholar] [CrossRef]
  57. Melão, M.G.G.; Rocha, O. Macrofauna Associada a Metania spinata (Cárter, 1881), Porifera, Metaniidae. Acta Limnol. Bras. 1996, 8, 59–64. [Google Scholar]
  58. De Roque, F.O.; Trivinho-Strixino, S.; Couceiro, S.R.M.; Hamada, N.; Volkmer-Ribeiro, C.; Messias, M.C. Species of Oukuriella Epler (Diptera, Chironomidae) inside Freshwater Sponges in Brazil. Rev. Bras. Entomol. 2004, 48, 291–292. [Google Scholar] [CrossRef]
  59. Fusari, L.M.; Roque, F.O.; Hamada, N. Sponge-Dwelling Chironomids in the Upper Paraná River (Brazil): Little Known but Potentially Threatened Species. Neotrop. Entomol. 2008, 37, 522–527. [Google Scholar] [CrossRef] [Green Version]
  60. Fusari, L.M.; Roque, F.O.; Hamada, N. Oukuriella Pesae, a New Species of Sponge-Dwelling Chironomid (Insecta: Diptera) from Amazonia, Brazil. Zootaxa 2009, 2146, 61–68. [Google Scholar] [CrossRef]
  61. Fusari, L.M.; Oliveira, C.S.N.; Hamada, N.; Roque, F.O. New Species of Ablabesmyia Johannsen from the Neotropical Region: First Report of a Sponge-Dwelling Tanypodinae. Zootaxa 2012, 3239, 43–50. [Google Scholar] [CrossRef]
  62. Fusari, L.M.; Bellodi, C.F.; Lamas, C.J.E. A New Species of Sponge-Dwelling Oukuriella (Chironomidae) from Brazil. Zootaxa 2014, 3764, 418. [Google Scholar] [CrossRef] [Green Version]
  63. Clavier, S.; Guillemet, L.; Rhone, M.; Thomas, A. First Report of the Aquatic Genus Climacia McLachlan, 1869 in French Guiana (Neuroptera, Sisyridae). Ephemera 2011, 12, 31–36. [Google Scholar]
  64. Hamada, N.; Pes, A.M.O.; Fusari, L.M. First Record of Sisyridae (Neuroptera) in Rio De Janeiro State, Brazil, with Bionomic Notes on Sisyra Panama. Fla. Entomol. 2014, 281–284. [Google Scholar] [CrossRef]
  65. Bowles, D. New Distributional Records for Neotropical Spongillaflies (Neuroptera: Sisyridae). Insecta Mundi 2015, 0400, 1–7. [Google Scholar]
  66. Ardila-Camacho, A.; Martins, C.C. First Record of Spongillaflies (Neuroptera: Sisyridae) from Colombia. Zootaxa 2017, 4276, 129–133. [Google Scholar] [CrossRef] [PubMed]
  67. Assmar, A.C.; Salles, F.F. Taxonomic and Distributional Notes on Spongilla-Flies (Neuroptera: Sisyridae) from Southeastern Brazil with First Interactive Key to the Species of the Country. Zootaxa 2017, 4273, 80–92. [Google Scholar] [CrossRef]
  68. Fisher, M.L.; Mower, R.C.; Nelson, C.R. Climacia Californica Chandler, 1953 (Neuroptera: Sisyridae) in Utah: Taxonomic Identity, Host Association and Seasonal Occurrence. Aquat. Insects 2019, 40, 317–327. [Google Scholar] [CrossRef] [Green Version]
  69. Da Fernandes, I.S.; Nicacio, G.; Rodrigues, G.G.; Silva, F.L. da Freshwater Sponge-Dwelling Chironomidae (Insecta, Diptera) in Northeastern Brazil. Biotemas 2019, 32, 39–48. [Google Scholar] [CrossRef]
  70. Brown, H.P. The Life History of Climacia areolaris (Hagen), a Neuropterous “Parasite” of Fresh Water Sponges. Am. Midl. Nat. 1952, 47, 130–160. [Google Scholar] [CrossRef]
  71. Parfin, S.I.; Gurney, A.B. The Spongilla-Flies, with Special Reference to Those of the Western Hemisphere (Sisyridae, Neuroptera). Proc. U. S. Natl. Mus. 1956, 105, 421–529. [Google Scholar] [CrossRef] [Green Version]
  72. Roback, S.S. Insects Associated with the Sponge Spongilla fragilis in the Savannah River. Not. Nat. 1968, 412, 1–10. [Google Scholar]
  73. Heiman, D.R.; Knight, A.W. A North American Trichopteran Larva Which Feeds on Freshwater Sponges (Trichoptera: Leptoceridae; Porifera: Spongillidae). Am. Midl. Nat. 1970, 84, 278–280. [Google Scholar] [CrossRef]
  74. Poirrier, M.A. Some Fresh-Water Sponge Hosts of Louisiana and Texas Spongilla-Flies, with New Locality Records. Am. Midl. Nat. 1969, 81, 573–575. [Google Scholar] [CrossRef]
  75. Poirrier, M.A.; Arceneaux, Y.M. Studies on Southern Sisyridae (Spongilla-Flies) with a Key to the Third-Instar Larvae and Additional Sponge-Host Records. Am. Midl. Nat. 1972, 88, 455–458. [Google Scholar] [CrossRef]
  76. Resh, V.H. Life Cycles of Invertebrate Predators of Freshwater Sponge. In Aspects of Sponge Biology; Harrison, F.W., Cowden, R.R., Eds.; Academic Press: New York, NY, USA, 1976; pp. 299–314. ISBN 978-0-12-327950-7. [Google Scholar]
  77. Pennak, R.W. Fresh-Water Invertebrates of the United States, 2nd ed.; John Wiley & Sons: Hoboken, NJ, USA; Ronald Press: New York, NY, USA, 1978. [Google Scholar]
  78. Matteson, J.D.; JacobiI, G.Z. Benthic Macroinvertebrates Found on The Freshwater Sponge Spongilla lacustris. Gt. Lakes Entomol. 1980, 3, 162–172. [Google Scholar]
  79. Stoaks, R.D.; Neel, J.K.; Post, R.L. Observations on North Dakota Sponges (Haplosclerina: Spongillidae) and Sisyrids (Neuroptera: Sisyridae). Gt. Lakes Entomol. 1983, 16, 171–176. [Google Scholar]
  80. Clark, W.H. First Record of Climacia Californica (Neuroptera: Sisyridae) and Its Host Sponge, Ephydatia mulleri (Porifera: Spongillidae), from Idaho with Water Quality Relationships. Gt. Basin Nat. 1985, 45, 2. [Google Scholar]
  81. Pupedis, R.J. Foraging Behavior and Food of Adult Spongila-Flies (Neuroptera: Sisyridae). Ann. Entomol. Soc. Am. 1987, 80, 758–760. [Google Scholar] [CrossRef]
  82. Whitlock, H.N.; Morse, J.C. Ceraclea Enodis, a New Species of Sponge-Feeding Caddisfly (Trichoptera: Leptoceridae) Previously Misidentified. J. North Am. Benthol. Soc. 1994, 13, 580–591. [Google Scholar] [CrossRef]
  83. Bowles, D.E. Spongillaflies (Neuroptera: Sisyridae) of North America with a Key to the Larvae and Adults. Zootaxa 2006, 1357, 1–19. [Google Scholar]
  84. Cover, M.R.; Resh, V.H. Global Diversity of Dobsonflies, Fishflies, and Alderflies (Megaloptera; Insecta) and Spongillaflies, Nevrorthids, and Osmylids (Neuroptera; Insecta) in Freshwater. In Freshwater Animal Diversity Assessment; Developments in Hydrobiology; Balian, E.V., Lévêque, C., Segers, H., Martens, K., Eds.; Springer: Dordrecht, The Netherlands, 2008; pp. 409–417. ISBN 978-1-4020-8259-7. [Google Scholar]
  85. Rothfuss, A.H.; Heilveil, J.S. Distribution of Sisyridae and Freshwater Sponges in the Upper-Susquehanna Watershed, Otsego County, New York with a New Locality for Climacia areolaris (Hagen). Am. Midl. Nat. 2018, 180, 298–305. [Google Scholar] [CrossRef]
  86. Bowles, D.E.; Courtney, G.W. The Aquatic Neuropterida of Iowa. Proc. Entomol. Soc. Wash. 2020, 122, 556–565. [Google Scholar] [CrossRef]
  87. Vogel, S. Current-Induced Flow through Living Sponges in Nature. Proc. Natl. Acad. Sci. USA 1977, 74, 2069–2071. [Google Scholar] [CrossRef] [Green Version]
  88. Frost, T.M. Clearance Rate Determinations for the Fresh Water Sponge Spongilla Lacustris Effects of Temperature Particle Type and Concentration and Sponge Size. Arch. Hydrobiol. 1980, 90, 330–356. [Google Scholar]
  89. Hanjavanit, C.; Tangpirotewong, N. Comparison of Benthic Macroinvertebrate Community Structure in Relation to Different Types of Human Disturbance along the Pong River, Khon Kaen Province (Thai). Asia-Pac. J. Sci. Technol. 2007, 12, 402–419. [Google Scholar]
  90. Annandale, N. Freshwater Sponges, Hydroids and Polyzoa. In The Fauna of British India, including Ceylon and Burma; Shipley, A.E., Ed.; Taylor and Francis: London, UK, 1911; pp. 49–94. [Google Scholar]
  91. Koukouras, A.; Russo, A.; Voultsiadou-Koukoura, E.; Arvanitidis, C.; Stefanidou, D. Macrofauna Associated with Sponge Species of Different Morphology. Mar. Ecol. 1996, 17, 569–582. [Google Scholar] [CrossRef]
  92. Neves, G.; Omena, E. Influence of Sponge Morphology on the Composition of the Polychaete Associated Fauna from Rocas Atoll, Northeast Brazil. Coral Reefs 2003, 22, 123–129. [Google Scholar] [CrossRef]
  93. Boon, P.J. Adaptive Strategies of Amphipsyche Larvae (Trichoptera: Hydropsychidae) Downstream of a Tropical Impoundment. In The Ecology of Regulated Streams; Springer: Berlin/Heidelberg, Germany, 1979; pp. 237–255. [Google Scholar]
  94. De Oliveira Roque, F.; Trivinho-Strixino, S. Xenochironomus ceciliae (Diptera: Chironomidae), a New Chironomid Species Inhabiting Freshwater Sponges in Brazil. Hydrobiologia 2005, 534, 231–238. [Google Scholar] [CrossRef]
  95. Sata, N.U.; Kaneniwa, M.; Masuda, Y.; Ando, Y.; Iida, H. Fatty Acid Composition of Two Species of Japanese Freshwater Sponges Heterorotula multidentata and Sponilla alba. Fish. Sci. 2002, 68, 236–238. [Google Scholar] [CrossRef] [Green Version]
  96. Steffan, A.W. Ectosymbiosis in aquatic insects. In Symbiosis; Henry, M.S., Ed.; Academic Press: New York, USA, 1967; pp. 207–289. [Google Scholar]
  97. Sangpradub, N.; Inmuong, Y.; Hanjavanit, C.; Inmuong, U. Biotic Indices for Biological Classification of Water Quality in the Pong Catchment Using Benthic Macroinvertebrates. KKU Sci. J. 1998, 6, 289–304. [Google Scholar]
  98. Sriariyanuwath, E.; Sangpradub, N.; Hanjavanit, C. Diversity of Chironomid Larvae in Relation to Water Quality in the Phong River, Thailand. Aquac. Aquar. Conserv. Legis. 2015, 8, 933–945. [Google Scholar]
  99. Weissmair, W.; Waringer, J. Identification of the Larvae and Pupae of Sisyra Fuscata (Fabricius, 1793) and Sisyra Terminalis Curtis, 1854 (Insecta: Planipennia: Sisyridae), Based on Austrian Material. Aquat. Insects 1994, 16, 147–155. [Google Scholar] [CrossRef]
  100. Navás, L. Névroptères et Insectes Voisins. Chine et Pays Environnants. 4e Série. Notes d'Entomologie Chinoise 1933, 1, 1–23. [Google Scholar]
  101. Lu, X.; Lin, A.; Wang, D.; Liu, X. The First Mitochondrial Genome of Spongillafly from Asia (Neuroptera: Sisyridae: Sisyra aurorae Navás, 1933) and Phylogenetic Implications of Osmyloidea. Mitochondrial DNA Part B 2021, 6, 2369–2370. [Google Scholar] [CrossRef] [PubMed]
  102. Monserrat, V.J. Sobre los Sisiridos de la Región Oriental (Neuroptera, Planipennia, Sisyridae). Rev. Esp. Entomol. 1982, 57, 165–186. [Google Scholar]
  103. New, T.R. The Neuroptera of Malesia; Brill: Leiden, Netherlands, 2003; 204p. [Google Scholar]
  104. Boon, P.J. Gastric Mill Structure and Its Phylogenetic Significance in Larval Hydropsychidae (Trichoptera). Zool. J. Linn. Soc. 1985, 84, 301–324. [Google Scholar] [CrossRef]
  105. Myers, N.; Mittermeier, R.A.; Mittermeier, C.G.; Da Fonseca, G.A.; Kent, J. Biodiversity Hotspots for Conservation Priorities. Nature 2000, 403, 853–858. [Google Scholar] [CrossRef] [PubMed]
  106. New Species Discoveries in The Greater Mekong. 2020. Available online: https://www.wwf.org.la/publications/new_species_discoveries_in_the_greater_mekong_2020/ (accessed on 1 September 2022).
  107. Ruengsawang, N.; Sangpradub, N.; Artchawakom, T.; Pronzato, R.; Manconi, R. Rare Freshwater Sponges of Australasia: New Record of Umborotula Bogorensis (Porifera: Spongillida: Spongillidae) from the Sakaerat Biosphere Reserve in Northeast Thailand. Eur. J. Taxon. 2017, 260, 1–24. [Google Scholar] [CrossRef] [Green Version]
  108. Calcinai, B.; Cerrano, C.; Núñez-Pons, L.; Pansini, M.; Thung, D.C.; Bertolino, M. A New Species of Spongilla (Porifera, Demospongiae) from a Karst Lake in Ha Long Bay (Vietnam). J. Mar. Sci. Eng. 2020, 8, 1008. [Google Scholar] [CrossRef]
  109. Bell, J.J.; McGrath, E.; Biggerstaff, A.; Bates, T.; Cárdenas, C.A.; Bennett, H. Global Conservation Status of Sponges. Conserv. Biol. 2015, 29, 42–53. [Google Scholar] [CrossRef]
  110. Tan, Y.-L.; Chen, J.-E.; Yiew, T.-H.; Habibullah, M.S. Habitat Change and Biodiversity Loss in South and Southeast Asian Countries. Environ. Sci. Pollut. Res. 2022, 29, 63260–63276. [Google Scholar] [CrossRef]
  111. Van Soest, R.W.; Boury-Esnault, N.; Vacelet, J.; Dohrmann, M.; Erpenbeck, D.; de Voogd, N.J.; Santodomingo, N.; Vanhoorne, B.; Kelly, M.; Hooper, J.N. Global Diversity of Sponges (Porifera). PLoS ONE 2012, 7, e35105. [Google Scholar] [CrossRef]
  112. Jones, C.G.; Lawton, J.H.; Shachak, M. Organisms as Ecosystem Engineers. In Ecosystem Management; Springer: Berlin/Heidelberg, Germany, 1994; pp. 130–147. [Google Scholar]
  113. Ormerod, S.J. A Golden Age of River Restoration Science? Aquat. Conserv. Mar. Freshw. Ecosyst. 2004, 14, 543–549. [Google Scholar] [CrossRef]
Diversity 14 00911 g001 550
Figure 1. Map of the Lower Mekong River hydrographic basin with the study site along Pong River (indicated by a red dashed-line square) in Northeastern Thailand, Southeast Asia (modified from van Zalinge et al. [18]).
Figure 1. Map of the Lower Mekong River hydrographic basin with the study site along Pong River (indicated by a red dashed-line square) in Northeastern Thailand, Southeast Asia (modified from van Zalinge et al. [18]).
Diversity 14 00911 g001
Diversity 14 00911 g002 550
Figure 2. View of the study site. (a) Corvospongilla siamensis on artificial substrata. (b) Schematic diagram of a raft, submerged structures, and nylon lines colonized by sponges (orange) at 0.3–1 m water depth in the study site.
Figure 2. View of the study site. (a) Corvospongilla siamensis on artificial substrata. (b) Schematic diagram of a raft, submerged structures, and nylon lines colonized by sponges (orange) at 0.3–1 m water depth in the study site.
Diversity 14 00911 g002
Diversity 14 00911 g003 550
Figure 3. Corvospongilla siamensis (Porifera: Spongillida) in vivo settled on the raft artificial substrata of Pong River (Lower Mekong). (a) Outline of sponge conulose body surface with a variety of microhabitats at level of irregularly scattered crevices and ridges, and tube-like exhalant aquiferous openings (oscules). (b) Caddisfly larvae (Amphipsyche meridiana, Hydropsychidae, Trichoptera) crawling on a cavity-rich surface of a greenish sponge. (c,d) Chironomid larvae (Chironomidae, Diptera) burrowing in the inner sponge body.
Figure 3. Corvospongilla siamensis (Porifera: Spongillida) in vivo settled on the raft artificial substrata of Pong River (Lower Mekong). (a) Outline of sponge conulose body surface with a variety of microhabitats at level of irregularly scattered crevices and ridges, and tube-like exhalant aquiferous openings (oscules). (b) Caddisfly larvae (Amphipsyche meridiana, Hydropsychidae, Trichoptera) crawling on a cavity-rich surface of a greenish sponge. (c,d) Chironomid larvae (Chironomidae, Diptera) burrowing in the inner sponge body.
Diversity 14 00911 g003
Diversity 14 00911 g004 550
Figure 4. Corvospongilla siamensis morphology (Pong River, Lower Mekong). (a,b) Heterogeneous microhabitat at the sponge irregular surface with ridges and large tube-like exhalant aquiferous aperture openings.
Figure 4. Corvospongilla siamensis morphology (Pong River, Lower Mekong). (a,b) Heterogeneous microhabitat at the sponge irregular surface with ridges and large tube-like exhalant aquiferous aperture openings.
Diversity 14 00911 g004
Diversity 14 00911 g005 550
Figure 5. Sponge-dwelling caddisfly and non-biting midge larvae recycling siliceous spicules of Corvospongilla siamensis (Lower Mekong, Southeast Asia). (a,b) Pupae case of spongivorous Amphipsyche meridiana (Trichoptera, Hydropsychidae) reinforced by megascleres and microscleres (arrows, SEM) adhering to the silk network of the inner and outer cases. (c,d) Case of a chironomid larva (Chironomidae, Diptera) with a dense network of spicules (arrow, LM).
Figure 5. Sponge-dwelling caddisfly and non-biting midge larvae recycling siliceous spicules of Corvospongilla siamensis (Lower Mekong, Southeast Asia). (a,b) Pupae case of spongivorous Amphipsyche meridiana (Trichoptera, Hydropsychidae) reinforced by megascleres and microscleres (arrows, SEM) adhering to the silk network of the inner and outer cases. (c,d) Case of a chironomid larva (Chironomidae, Diptera) with a dense network of spicules (arrow, LM).
Diversity 14 00911 g005
Diversity 14 00911 g006 550
Figure 6. Eggs of Povilla heardi (Ephemeroptera, Polymitarcyidae) on Corvospongilla siamensis (Lower Mekong, Southeast Asia). (a) Egg jelly envelopes (arrows) on the irregular surface of a live sponge. (b) Eggs viewed by light microscopy.
Figure 6. Eggs of Povilla heardi (Ephemeroptera, Polymitarcyidae) on Corvospongilla siamensis (Lower Mekong, Southeast Asia). (a) Egg jelly envelopes (arrows) on the irregular surface of a live sponge. (b) Eggs viewed by light microscopy.
Diversity 14 00911 g006
Diversity 14 00911 g007 550
Figure 7. Occurrence and composition of sponge-dwelling larvae of aquatic insects associated with 14 samples of Corvospongilla siamensis (Pong River, Lower Mekong). One cluster comprised the shallow-water samples (0.3 m) and the other all but one of those from deep water (1 m).
Figure 7. Occurrence and composition of sponge-dwelling larvae of aquatic insects associated with 14 samples of Corvospongilla siamensis (Pong River, Lower Mekong). One cluster comprised the shallow-water samples (0.3 m) and the other all but one of those from deep water (1 m).
Diversity 14 00911 g007
Diversity 14 00911 g008 550
Figure 8. Amphipsyche meridiana (Trichoptera, Hydropsychidae) associated with Corvospongilla siamensis (Lower Mekong, Southeast Asia). (a,b) Scheme of body and digestive tract of the sponge-eating caddisfly larva (adapted from Sangpradub and Giller [27]). The position of the proventriculus (*) is indicated in (b). (c) Siliceous spicules with blunt tips (arrows) in the proventriculus. (d) Food debris in the midgut, i.e., diatoms and a rotifer.
Figure 8. Amphipsyche meridiana (Trichoptera, Hydropsychidae) associated with Corvospongilla siamensis (Lower Mekong, Southeast Asia). (a,b) Scheme of body and digestive tract of the sponge-eating caddisfly larva (adapted from Sangpradub and Giller [27]). The position of the proventriculus (*) is indicated in (b). (c) Siliceous spicules with blunt tips (arrows) in the proventriculus. (d) Food debris in the midgut, i.e., diatoms and a rotifer.
Diversity 14 00911 g008
Diversity 14 00911 g009 550
Figure 9. Dense assemblage of freshwater sponges with massive, irregular growth form as engineering species on farm nets in the Pong River (Lower Mekong, Southeast Asia). (a) The red area outlining the body of Corvospongilla siamensis is ~800 cm2. (b) Living Corvospongilla sp. with associated algae. (c) Dry freshwater sponges on net.
Figure 9. Dense assemblage of freshwater sponges with massive, irregular growth form as engineering species on farm nets in the Pong River (Lower Mekong, Southeast Asia). (a) The red area outlining the body of Corvospongilla siamensis is ~800 cm2. (b) Living Corvospongilla sp. with associated algae. (c) Dry freshwater sponges on net.
Diversity 14 00911 g009
Diversity 14 00911 g010 550
Figure 10. Fish cage maintenance after harvesting in the Pong River. (a) Fisherman with dried nets. (b,c) Freshwater sponges encrusting on farm nets.
Figure 10. Fish cage maintenance after harvesting in the Pong River. (a) Fisherman with dried nets. (b,c) Freshwater sponges encrusting on farm nets.
Diversity 14 00911 g010
Table
Table 1. Checklist of aquatic insects associated with Corvospongilla siamensis in the Pong River (Lower Mekong, Thailand). Total number of larvae and/or pupae in each sponge sample at two water depths. Presence of eggs is indicated by asterisk (*).
Table 1. Checklist of aquatic insects associated with Corvospongilla siamensis in the Pong River (Lower Mekong, Thailand). Total number of larvae and/or pupae in each sponge sample at two water depths. Presence of eggs is indicated by asterisk (*).
TaxaNumber of IndividualsTotal
Depth 0.3 mDepth 1.0 m
12345671234567
Ephemeroptera
  Baetidae gen. sp.-------1------1
  Caenidae
      Caenodes sp.-2---1--------3
  Polymitarcyidae
      Povilla heardi-------*-------
Neuroptera
  Sisyridae
      Sisyra sp.-31-1--2-11---9
Trichoptera
  Ecnomidae
      Ecnomus spp.-831414212712712192
  Hydropsychidae
      Amphipsyche meridiana-------6220----284
  Hydroptilidae gen. sp.-1-----411----7
  Trichoptera fam. gen.------1--1----2
Diptera
  Chironomidae
      Ablabesmyia sp.133111--------10
      Demicryptochironomus sp.-2----1-------3
      Dicrotendipes sp.-261211-----1-14
      Nanocladius sp.-----1-1----1-3
      Paramerina sp.-32---1---1-1-8
      Polypedilum sp.21295517348683376
      Rheotanytarsus sp.--------5121--9
      Tanytarsus sp.-1-2--2--1----6
      Xenochironomus sp.-91013-2-73321243
      Chironomidae gen. sp.-14-----1-11--8
  Ceratopogonidae
      Bezzia sp.---------1----1
Total347381116619946529211398379
Table
Table 2. Worldwide inventory of aquatic Insecta inhabiting Spongillida (Porifera) so far reported. Sponge species belong to families Lubomirskiidae, Metaniidae, Potamolepidae, and Spongillidae. Taxa and countries listed in alphabetical order. References listed in chronological order.
Table 2. Worldwide inventory of aquatic Insecta inhabiting Spongillida (Porifera) so far reported. Sponge species belong to families Lubomirskiidae, Metaniidae, Potamolepidae, and Spongillidae. Taxa and countries listed in alphabetical order. References listed in chronological order.
Insect TaxaSponge TaxaReferencesBiogeographic Region/Country
Ephemeroptera (Baetidae, Caenidae, Polymitarcyidae)
Neuroptera (Sisyridae)
Trichoptera (Ecnomidae, Hydroptilidae, Hydropsychidae)
Diptera (Ceratopogonidae, Chironomidae)		Corvospongilla siamensisPresent paper, Annandale [29], Schröder [30]Oriental-Himalayan
Thailand; Borneo; India; Java; Philippines
Eunapius carteri
Radiospongilla crateriformis
Spongilla alba
Spongillida fam. gen. sp.
---Spongilla albaSchröder [30], Mansell [31]Afrotropical
Madagascar; South Africa
Spongillida fam. gen. sp.
Trichoptera (Hydroptilidae)Spongillida fam. gen. sp.Wells [32], Wells & Johanson [33], Forteath & Osborne [34], Forteath et al. [35]Australasian
Australia; New Zealand;
New Caledonia; Tasmania
Diptera (Chironomidae)
Ephemeroptera (Baetidae, Caenidae)
Neuroptera (Sisyridae)
Megaloptera (Sialidae)
Trichoptera (Apataniidae, Brachycentridae, Ecnomidae,
Hydropsychidae, Hydroptilidae, Leptoceridae,
Limnephilidae, Polycentropodidae, Psychomyiidae)		Ephydatia fluviatilisPavesi [36], Arndt [37], Rezvoi [38], Berg [39], Gaumont [40], Moretti & Corallini-Sorcetti [41], Konopacka & Socinski [42], Kamaltynov et al. [43], Weissmair & Mildner [44], Gugel [45], Corallini & Gaino [46,47], Gaino et al. [48], Wallace et al. [49], Weinberg et al. [50], Loru et al. [51], Schiffels [52], Sokolova & Palatov [53], Palatov & Sokolova [54], Zvereva et al. [55], Ostrovsky [56]Palaearctic
Algeria; Austria; China; East Siberia; Denmark; England; France; Germany; Italy; Japan; Mongolia; Poland; Russia; Scandinavia; Serbia; Spain
Ephydatia muelleri
Eunapius fragilis
Heteromeyenia sp.
Lubomirskia baikalensis
Spongilla lacustris
Spongillida fam. gen. sp.
Diptera (Chironomidae, Simuliidae)
Coleoptera (Dytiscidae)
Ephemeroptera (Polymitarcyidae, Tricorythidae)
Hemiptera (Belostomatidae)
Lepidoptera (Pyralidae)
Neuroptera (Sisyridae)
Odonata (Coenagrionidae, Libellulidae)
Trichoptera (Hydropsychidae, Polycentropodidae)		Acalle recurvataMelão & Rocha [57], Roque et al. [58], Fusari et al. [59,60,61,62], Clavier et al. [63], Hamada et al. [64], Bowles [65], Ardila-Camacho & Martins [66], Assmar & Salles [67], Fisher et al. [68], da Silva Fernandes [69]Neotropical
Argentina; Belize; Bolivia; Brazil; Chile; Cuba; French Guiana; Guatemala; Guyana; Honduras; Mexico; Panama; Paraguay; Peru; Suriname; Uruguay; Venezuela
Drulia uruguayensis
Corvoheteromeyenia australis
Corvospongilla seckti
Heteromeyenia cristalina
Metania spinata
Metania reticulata
Oncosclera navicella
Oncosclera spinifera
Radiospongilla inesi
Trochospongilla paulula
Neuroptera (Sisyridae)
Megaloptera
Trichoptera (Leptoceridae)		Eunapius fragilisBrown [70], Parfin & Gurney [71], Roback [72], Heiman & Knight [73], Poirrier [74], Poirrier & Arceneaux [75], Resh [76], Pennak [77], Matteson & Jacobi [78], Stoakes et al. [79], Clark [80], Pupedis [81], Whitlock & Morse [82], Bowles [65,83], Cover & Resh [84], Rothfuss & Heilveil [85], Fisher et al. [68], Bowles & Courtney [86]Nearctic
United States of America
Canada
Ephydatia muelleri
Ephydatia fluviatilis
Eunapius igloviformis
Dosilia radiospiculata
Heteromeyenia argirosperma
Heteromeyenia baileyi
Heteromeyenia repens
(as H. baileyi)
Racekiela ryderi
(as Heteromeyenia ryderi)
Radiospongilla crateriformis
Spongilla lacustris
Ephydatia robusta
(as Meyenia subdivisa)
Trochospongilla horrida
Trochospongilla leidii
(as T. leidyi)
Trochospongilla muelleri
Trochospongilla pennsylvanica
(as Tubella pennsylvanica)
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Ruengsawang, N.; Sangpradub, N.; Manconi, R. Aquatic Insects in Habitat-Forming Sponges: The Case of the Lower Mekong and Conservation Perspectives in a Global Context. Diversity 2022, 14, 911. https://doi.org/10.3390/d14110911

AMA Style

Ruengsawang N, Sangpradub N, Manconi R. Aquatic Insects in Habitat-Forming Sponges: The Case of the Lower Mekong and Conservation Perspectives in a Global Context. Diversity. 2022; 14(11):911. https://doi.org/10.3390/d14110911

Chicago/Turabian Style

Ruengsawang, Nisit, Narumon Sangpradub, and Renata Manconi. 2022. "Aquatic Insects in Habitat-Forming Sponges: The Case of the Lower Mekong and Conservation Perspectives in a Global Context" Diversity 14, no. 11: 911. https://doi.org/10.3390/d14110911

APA Style

Ruengsawang, N., Sangpradub, N., & Manconi, R. (2022). Aquatic Insects in Habitat-Forming Sponges: The Case of the Lower Mekong and Conservation Perspectives in a Global Context. Diversity, 14(11), 911. https://doi.org/10.3390/d14110911

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop