Article

Allometric and trophic effects on shell morphology of Pomacea canaliculata (Caenogastropoda, Ampullariidae) from a geometric morphometrics viewpoint

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Abstract

Pomacea canaliculata, an invasive apple snail native to South America, is a serious pest of aquatic crops in several parts of the world. The origin of inter-population variation in shell shape is thought to be both genetic and environmental but the reaction norms to specific environmental factors are still poorly understood. Our aims were to analyze the existence of direct and indirect (allometric) effects of food availability (FA) on the shape of young adults of P. canaliculata. Full sibling hatchlings were reared under different levels of FA. Nine landmarks and 10 semi-landmarks were determined on photographs of mature shells and analyzed using geometric morphometrics. In both sexes significant allometry was found: a decrease in the spire height in both sexes, and an increase of the aperture size in males and of the last whorl in females. When this allometric component was removed a relationship between size-corrected shape and FA was found only in females, which were more globose and had a larger aperture when grown under high FA. This effect may be explained by the faster growth of the reproductive organs and the thinner shells of the best fed females.

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... temperature, Zdelar et al., 2017), or in resources (e.g. food availability, Tamburi and Martín, 2013). Information on the influence of temperature on freshwater snails is important for understanding and predicting changes in their distribution and performance in the face of global climate change (Tomanek, 2008), especially in traits exhibiting great plasticity. ...
... Following the geometric morphometrics methodology previously applied in this species (detailed by Tamburi and Martín, 2013), 9 landmarks ( Fig. 1; Bookstein, 1997) were digitized using TPSdig2 software (Rohlf, 2017). Landmark 1 (LM 1) is the apex of the shell; LM 2 and 8 are left and right intersections of the last complete suture in the shell outline; LM 3 is the upper suture between the body whorl and the aperture; LM 4 is the most external point of the aperture on the left margin and LM 7 is the most external point of the body whorl on the right margin of the shell; LM 5 is the extreme point of the aperture border opposite to the apex; LM 6 is the intersection of the aperture border and the outline of the body whorl; LM 9 is the intersection of the umbilicus border and the aperture border. ...
... Multivariate tests of Pillai's trace were used because of unequal and small sample sizes in some treatments (Zar, 1984). When these results were significant, the subsequent analyses were performed using the residual values of the pooled within groups regression between shape and size, defined as allometry corrected shape (ACS), to explore shape changes separately from allometry (Tamburi and Martín, 2013). Allometric trajectories of the snails reared at different temperatures were compared within each sex to validate a global correction for allometry. ...
Article
Temperature has a great influence on the life-history traits of freshwater snails. In this study we investigated the long term effects of a range of temperatures on shell morphology of the apple snail Pomacea canaliculata, a highly invasive species and an important pest of rice. Analysis of shells using geometric morphometrics showed that the main source of morphological variation was allometry, which was detected in males but not in females. This intersexual divergence in allometric trajectories generates much of the morphological variation evidenced. In females, the monotonic relationship with temperature produced narrower shells in the snails reared at lower temperatures, and more expanded apertures, relatively bigger than the body whorl, at higher temperatures. We also found an inverse relationship between relative shell weight, a proxy for shell thickness, and temperature. The differences in shape and relative shell weight are attributable to the different growth rates associated with different temperatures. Temperature fluctuation around a mean of 23.2 °C seemed to have no influence in shell shape and relative weight when is compared with a constant temperature of 25 °C. Information on the influence of temperature on freshwater snails is important for understanding and predicting changes in the face of global climatic change, especially in traits exhibiting great plasticity, such as shell shape and thickness. This work showed that higher temperatures could result in a relatively thinner shell, implying a greater significance of corrosion in flowing waters and a lower resistance to crushing by predators, especially in low latitude areas.
... Likewise, several studies on growth, survival, respiration, and abiotic tolerance of Pomacea spp. which were highly dependent on healthy animals, indicate that snails were reared exclusively on plant material which may have led to unhealthy animals and questionable experimental results (Seuffert and Martin, 2008;Tamburi and Martin, 2008;Seuffert and Martin, 2010;Seuffert and Martin, 2013;Tamburi and Martin, 2013;. ...
... Snails in LA are likely to encounter drought, flooding, seasonal variation in food, and competition that may select for hardier snails that are more tolerant to environmental extremes. Temperature and starvation have been reported to affect development of P. canaliculata in respect to mortality, growth, size, maturation, fecundity, shell morphology, inter-clutch interval, and longevity (Estebenet and Cazzaniga, 1992;Tamburi and Martin, 2009;Tamburi and Martin, 2013;Seuffert and Martin, 2013). Donnay and Beissinger (1993) reported that water conditions affected the size, fecundity, and juvenile survival rate in Pomacea doliodes. ...
Thesis
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Apple snails are in the Family Ampullariidae, a family of freshwater gastropods. Some species in the genus Pomacea have gained considerable notoriety as very destructive invasive species. Ampullariids have a gill and breathe water; in some species, the mantle cavity is modified into an air sack that may function as a lung or flotation device. Apple snails definitively identified as Pomacea maculata have successfully invaded numerous localities in Louisiana, and studies of the physiology of these animals may enhance our understanding of the biology of highly invasive species and suggest effective approaches to controlling the invasive populations. This study investigated respiration of P. maculata in water and in air and the ability of the animals to survive long-term emersion in a state of aestivation. The ability of the animals to disperse over dry ground was studied. Finally, the anatomy of the gill and lung were examined. The results of the study indicate that the gill and the lung in P. maculata are vascularized, capable of gas exchange, and fully functional, which permits survival and respiration in water and during long- and short-term exposure to air. Both the capacity to sustain travel over dry land and the ability to survive long term aerial exposure in an aestivated state were demonstrated by P. maculata. The major physiological changes observed during aestivation include a decrease in heart rate, a reduction in VO2, and the use of discontinuous respiration. A review of published literature suggests that extensive physiological variation exists among populations of native and invasive P. maculata. In conclusion, P. maculata in Louisiana is well-adapted to life in both water and air, can move overland, and can survive emersion for over a year. These physiological adaptations suggest that controlling the further spread of P. maculata will be very difficult.
... In each picture, a total of 19 landmarks (Fig. 2) were set following previous studies (Tamburi & Martín, 2013); nine true landmarks and ten sliding semi-landmarks were digitalized using TPSdig2 software (Rohlf, 2010). Landmark 1 is the apex of the shell; landmarks 2 and 18 are left and right intersections of the last complete suture in the shell outline; landmark 3 is the upper suture between the body whorl and the aperture; landmarks 6 and 15 are the most external point of the aperture on the left margin and the most external point of the body whorl on the right margin of the shell, respectively; landmark 9 is the extreme point of the aperture border opposite the apex, and landmark 12 is the intersection of the aperture border and the outline of the body whorl; landmark 19 is the umbilicus of the shell. ...
... In our study, the anti-clockwise specimens were located on the same side of the morphometric cloud relative to the consensus configuration of each population but were not extreme in their position. At least in the Corto stream population, the similarity in the shell shape of the two anti-clockwise males seems to be related to shared sexually dimorphic characteristics (Tamburi & Martín, 2013) and not to their coiling direction. ...
Article
Snails exhibit a primary left-right asymmetry that appears during the first cleavages of the eggs, and a secondary asymmetry, related to the coiling of the shell. Most species are constituted by either dextral or sinistral morphs (enantiomorphs) while individuals with reversed primary asymmetry are extremely rare. Freshwater snails of the family Ampullariidae are normally dextral enantiomorphs with planispiral, hyperstrophic or orthostrophic shells. Pomacea canaliculata, a well-studied species because of its invasive status, shows dextral primary asymmetry and orthostrophic growth that results in clock-wise shells. Despite the great number of studies focused on P. canaliculata, only two specimens with reversed asymmetry have been hitherto reported. Here we report the finding of two live snails and three empty shells of P. canaliculata with anti-clockwise coiling that appeared in two populations from the southern Pampas, Argentina. Both anti-clockwise live snails were males that attempted to copulate with clock-wise females in the laboratory but failed to inseminate them. The apex of anti-clockwise shells and the anatomy of the snails revealed that the reversal of coiling was due to an orthostrophic development of sinistral enantiomorphs. Morphological analysis performed through geometric morphometrics did not find other differences with clock-wise snails other than coiling direction. We conclude that these anti-clockwise snails are probably engendered, as in other snails species, when the mother is a recessive homozygote for reversing alleles that show delayed maternal inheritance. The chances of establishment of populations with dimorphic asymmetry are very low because of the reproductive disadvantages of anti-clockwise individuals.
... Hanning (1979) showed sexual dimorphism in some populations of P. paludosa (Say, 1829). The shell of P. canaliculata has been studied recently using geometric morphometrics (Tabugo et al., 2010;Torres et al., 2011;Moneva et al., 2012;Tamburi & Martín, 2013) to disentangle the relationship between size and shape. Both sexes exhibit static allometry (i.e., adults at the same stage of maturity but of different sizes have different shapes); spire height decreases with size in both sexes, whereas aperture and body whorl size increase with size in males and females, respectively (Tamburi & Martín, 2013). ...
... The shell of P. canaliculata has been studied recently using geometric morphometrics (Tabugo et al., 2010;Torres et al., 2011;Moneva et al., 2012;Tamburi & Martín, 2013) to disentangle the relationship between size and shape. Both sexes exhibit static allometry (i.e., adults at the same stage of maturity but of different sizes have different shapes); spire height decreases with size in both sexes, whereas aperture and body whorl size increase with size in males and females, respectively (Tamburi & Martín, 2013). ...
Article
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Apple snails (Ampullariidae) are among the largest and most ecologically important freshwater snails. The introduction of multiple species has reinvigorated the field and spurred a burgeoning body of research since the early 1990s, particularly regarding two species introduced to Asian wetlands and elsewhere, where they have become serious agricultural pests. This review places these recent advances in the context of previous work, across diverse fields ranging from phylogenetics and biogeography through ecology and developmental biology, and the more applied areas of environmental health and human disease. The review does not deal with the role of ampullariids as pests, nor their control and management, as this has been substantially reviewed elsewhere. Despite this large and diverse body of research, significant gaps in knowledge of these important snails remain, particularly in a comparative framework. The great majority of the work to date concerns a single species, Pomacea canaliculata, which we see as having the potential to become a model organism in a wide range of fields. However, additional comparative data are essential for understanding this diverse and potentially informative group. With the rapid advances in genomic technologies, many questions, seemingly intractable two decades ago, can be addressed, and ampullariids will provide valuable insights to our understanding across diverse fields in integrative biology.
... Landmark-based geometric morphometric features have been effectively used to characterize shape and size variation across populations in a wide diversity of Mollusca and ecological contexts (e.g., Teso et al. 2011;Dunithan et al. 2012;Tamburi & Martín, 2013;Yuvero & Giménez 2021;Doyle et al. 2022). Polyplacophorans, in particular have a body outline that is covered by the mantle girdle, which delineates an ellipse but hides access to anatomical landmarks (such as shallow notches on the lateral margins of each sclerite). ...
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The class Polyplacophora (chitons) represents a dorsoventrally flattened mollusk group that has an oval-shaped body covered with eight overlapping sclerites providing bilateral symmetry. Chitons show abnormalities (teratologies) that are characterized by symmetry deviations between the right and left sides of their bodies. As these deviations do not result in damage that affects vital functions, chitons are able to reach adult stages. In this study, we quantify the asymmetric condition of the species Chiton articulatus using a landmark-based geometric morphometric approach to assess variation in shape and bilateral symmetry. A geometric configuration of 22 landmarks and 50 semi-landmarks was created to evaluate shape variation in abnormal and deformed specimens compared to normal Chiton articulatus specimens. Vectors of change in the body shape configurations of chitons indicate that the greatest change occurs in the anterior part of the body, with less change in the middle and posterior parts. This gives chitons a widened appearance and provides anatomic compensation to restore the bilateral symmetry of the body scleritome. The diverse abnormalities and deformities had little impact on shape variations and confirmed that the coalescence condition is an intermediate step between a normal condition and the abnormal conditions of hypomerism or hypermerism. The low levels of fluctuating asymmetry expressed in C. articulatus indicate that despite living in areas of high stress, such as the rocky intertidal coast, this species maintains stability in its development and shape. Our results can serve as a model for studying bilateral symmetry deviation in polyplacophorans.
... A total of 174 representative shells were photographed for the geometric morphometric analysis. Following Tamburi & Martín (2013) and Rama Rao et al. (2018), a total of 19 landmarks were digitized using ImageJ v. 1.52a (Schneider, Rasband & Eliceiri, 2012) (Fig. 2). The package MorphoJ v. 1.06d (Klingenberg, 2011) was then used to run the geometric morphometric analysis. ...
Article
Ampullariidae include the largest of all freshwater snails and are of ecological, evolutionary and anthropogenic importance in Southeast Asia (SEA). Native ampullariids belonging to the genus Pila face various threats but are understudied, with their species taxonomy being confused and data on their distributions being scarce. We provide a comprehensive update on the nomenclature, status and distribution of Pila species in Thailand, based on DNA barcoding and geometric morphometric analysis of recently collected material. We confirm that at least five Pila species are extant in Thailand: Pila virescens, P. celebensis, P. turbinis, P. gracilis and P. pesmei. Pila celebensis, which has distinctive egg masses among all the known Southeast Asian Pila, appears to be sister to a clade comprising other SEA and some African Pila. Our results suggest that Pila may have dispersed into SEA on at least two separate occasions. Two singletons collected from northern and eastern Thailand may constitute separate species, but this requires further study. Intraspecific diversity of the mitochondrial cytochrome c oxidase subunit I gene was relatively high for P. celebensis, P. gracilis and P. pesmei (maximum uncorrected p-distances varied from 7% to 9%), and may include cryptic species. Conversely, P. virescens showed low intraspecific p-distances (c. 0%) among clades collected from different localities. This strongly suggests that introductions by humans may be the major cause of this pattern, and our own observations—we found that this species is being cultured and is commonly sold in markets for human consumption—are consistent with this. Pila turbinis was the rarest species, with live snails being collected from only two localities. Throughout Thailand, invasive confamilial Pomacea species appear to be replacing native Pila species, particularly in the Chao Phraya basin. While Thai Pila exhibit surprisingly high genetic diversity, with cryptic species likely being present, widespread invasive snails pose a major threat to their survival and urgent conservation action is needed.
... Our results were similar that the C content of snails increased significantly under high CO 2 conditions (Fig. 5a). Johannesson (1986) found that Littorina saxatilis with smaller aperture were more conducive to avoiding predation, and studies have found that female Pomacea canaliculata displayed a more expanded aperture at higher temperature and greater food availability and performed an increase in growth rates (Tamburi and Martín 2013). Our results indicated that the aperture width of snail was wider under high CO 2 conditions. ...
Article
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Aquatic plants and associated herbivores are expected to perform better under the rising atmospheric CO2 concentration brought about by climate change. However, it is not clear how increasing CO2 affects herbivory on aquatic macrophytes. In this research, we set four treatments (A group: ambient air without snails; AS group: ambient air with snails; E group: elevated CO2 without snails; and ES group: elevated CO2 with snails) and studied the effects of low (0–0.5 mg/L) and high (4–8 mg/L) CO2 concentration on the growth, morphology, and chemical traits of the macrophyte Vallisneria spiralis (Angiosperms: Hydrocharitaceae) and the snail Radix auricularia (Pulmonata: Lymnaeidae), and the relationships between them in the laboratory. We found that herbivory decreased the total biomass of V. spiralis by 28.6% and 25.3% under low and high CO2 conditions, respectively. Compared with A group, ES group reduced the total plant biomass by 43.3%. Elevated CO2 and herbivory both affected the growth of V. spiralis and change its resource allocation patterns. Total nitrogen content in V. spiralis leaves decreased under herbivory condition, and total phenols increased under the interactions condition between elevated CO2 and herbivory. However, total C content of R. auricularia increased under elevated CO2 condition. These results could provide valuable insights into how climate change affects plant–herbivore interactions and food web structure in shallow inland waters.
... Interpretation of trophic effects on shell shape is complicated by the allometric growth of the shell of P. canaliculata (Estebenet et al., 2006) and the effect of food availability on size at maturity (Tamburi & Martín, 2009b). Using geometric morphometrics techniques based on landmarks a significant static allometry (shape differences among adults of different size) has been detected in P. canaliculata (Tamburi & Martín, 2013). After statistically removing the allometric effects, only females showed a direct trophic effect on shell shape, being more globose and with a larger aperture when grown at high food availabilities. ...
Chapter
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Pomacea canaliculata is in many respects the best known species of apple snails (family Ampullariidae), although the available information is both fragmentary and geographically biased. Most studies in its non-native range have focused on applied aspects in managed or artificial wetlands in various countries in Southeast Asia. In its natural range the emphasis has been on basic studies of its reproductive biology, ecology and behaviour in populations from small streams at the southernmost extreme of its distribution (Southern Pampas, Argentina). The extreme geographic position and the lotic nature of these populations may have biased some conclusions about the behavioural and ecological traits of P. canaliculata; contemporary evolution and genetic exchange may also have diversified these traits in the non-native range. Even though the ecological information from native populations may not be directly applicable elsewhere, it nevertheless remains as a necessary reference to understand the full potential of adaptation and spread of P. canaliculata to new environments around the world. Surprisingly enough, comparative studies of native and non-native populations of Pomacea spp. are almost lacking. This short review focuses on the distribution, thermal biology, aerial respiration, feeding, reproduction, phenotypic plasticity and shell shape of Pomacea canaliculata in its native range in Argentina.
... Feeding perches were cleared of any shells before the beginning of the study. Shells were sexed based on aperture shape differences (Estebenet et al. 2006;Tamburi and Martín 2013), and their length measured and analysed using size classes. ...
Article
Snail Kites (Rostrhamus sociabilis) feed almost exclusively on Apple Snails (Pomacea spp.). While field observations indicate they discard the noxious albumen gland (AG) when feeding on female snails, there is no information on the energy lost by this behavior, the gland composition, or if there are snail sex preferences associated. We addressed for the first time these aspects for Snail Kites foraging on Pomacea canaliculata in southern South America. Whole snail’s biochemical composition exhibited significant differences between sexes. Proteins and carbohydrates were the major energy-providing components. Soft parts provide ~2.91±0.16 and 2.50±0.14 Kcal g-1 dw for male and female without AG, respectively while AG accounts for 15 % of available energy. Size and sex of prey consumed, determined at foraging perches sampled monthly, showed that Kites preferentially feed on the largest snails available throughout the sampling period. Even though the remains of female body without the AG have less energy than males, sex preferential predation toward females was observed. Our study demonstrates for the first time the optimal foraging trade-off between prey size/sex and nutrition/energy in Snail Kites. After discarding the albumen gland, male and female snails of equivalent size provide different nutrients and energy, though Snail Kite foraging is generally biased toward females mostly due to their bigger size suggesting Snail Kites are unable to distinguish between sex.
... Limited information is available on life-history traits of the Pomacea canaliculata (Lamarck, 1822) populations living in stable water bodies such as rivers and canals. To date, information on populations of this snail in such habitats has been restricted mainly to distribution (Martín, Estebenet & Cazzaniga, 2001;Seuffert & Martín, 2013a), morphology (Estebenet, Martín & Burela, 2006;Tamburi & Martín, 2013) and overwintering success (Ozawa & Makino, 1988;Ito, 2002). ...
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Seasonal variations in the morphology of the parenchymal mass and function of the albumen gland/capsule gland complex have been studied in Pomacea canaliculata, together with the cellular types involved in the synthesis and secretion of perivitellin fluid components. The two major parenchymal cell types, albumen secretory cells (AS) and labyrinthic cells (LC), undergo seasonal variations throughout the annual reproductive cycle, which is divided into three periods. Both cellular types show maximal development and structural complexity during the reproductive period (spring and summer). AS cells have a well-developed Golgi complex and rough endoplasmic reticulum and their secretory granules show electron-dense particles of about 20 nm (probably galactogen). These cells are uniquely involved in ovorubin and PV2 perivitellin synthesis and their secretory granules are the single storage site for these two major perivitellins, as revealed by immunoelectron microscopy. AS also possess calcium deposits that infiltrate the cytoplasmic matrix. The luminal surfaces of LC exhibit long cilia intermingled with sparce short microvilli. Basally, the plasma membrane shows deep irregular folds that extend through the cytoplasm up to the subapical region. Calcium deposits infiltrate the cytoplasm and accumulate in the extracellular space of the basal labyrinth. Nerve terminals seem to be involved in the regulation of parenchymal cell secretion. At the post-reproductive period, AS markedly change their aspect following the release of most of the secretory granules into the acinar lumen. LC decrease in volume, the number of their cilia decreases, their cytoplasmic folds are much thinner and their extracellular spaces lack calcium particles. At the pre-reproductive period (winter), AS and LC recover and prepare for the subsequent period.
Article
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Since the mid 1990s populations of non-native apple snails (Ampullariidae) have been discovered with increasing frequency in the continental United States. Given the dramatic effects that introduced apple snails have had on both natural habitats and agricultural areas in Southeast Asia, their introduction to the mainland U.S. is cause for concern. We combine phylogenetic analyses of mtDNA sequences with examination of introduced populations and museum collections to clarify the identities, introduced distributions, geographical origins, and introduction histories of apple snails. Based on sampling to date, we conclude there are five species of non-native apple snails in the continental U.S. Most significantly, we recognize three species within what has been called the channeled apple snail: Pomacea canaliculata (California and Arizona), Pomacea insularum, (Florida, Texas, and Georgia) and Pomacea haustrum (Florida). The first established populations of P. haustrum were discovered in the late 1970s in Palm Beach County Florida, and have not spread appreciably in 30 years. In contrast, populations of P. insularum were established in Texas by 1989, in Florida by the mid to late 1990s, and in Georgia by 2005, and this species continues to spread rapidly. Most introduced P. insularum haplotypes are a close match to haplotypes from the Río Uruguay near Buenos Aires, indicating cold tolerance, with the potential to spread from Florida, Georgia, and Texas through Louisiana, Alabama, Mississippi, and South Carolina. Pomacea canaliculata populations were first discovered in California in 1997. Haplotypes of introduced P. canaliculata match native-range haplotypes from near Buenos Aires, Argentina, also indicating cold tolerance and the potential to establish farther north. The term "channeled apple snail" is descriptive of a morphology found in many apple snail species. It does not identify a single species or a monophyletic group. Clarifying species identifications permits a more accurate assessment of introduction histories and distributions, and provides a very different picture of the tempo and pattern of invasions than was inferred when the three species with channeled sutures were considered one. Matching introduced and native-range haplotypes suggests the potential for range expansion, with implications for native aquatic ecosystems and species, agriculture, and human health.
Chapter
This 19-chapter book discusses the biology (including reproduction, life history, feeding preferences and sexual behaviour) of molluscs as pests of horticultural, field and fodder crops, and outlines the development of appropriate mechanisms for the control of these pests (mainly biological, cultural and chemical). Two chapters review progress towards the development of chemical control strategies, one addressing the toxicology of chemicals, the other the deployment of molluscicides in baits. These chapters also highlight the statistical and biological procedures for screening and evaluating molluscicides which are not a component of the standard procedure of mollusc control. A series of chapters focus on specific crop situations, providing a synopsis of the current pest status of gastropod species or species groups.
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Morphometrics, a new branch of statistics, combines tools from geometry, computer graphics and biometrics in techniques for the multivariate analysis of biological shape variation. Although medical image analysts typically prefer to represent scenes by way of curving outlines or surfaces, the most recent developments in this associated statistical methodology have emphasized the domain of landmark data: size and shape of configurations of discrete, named points in two or three dimensions. This paper introduces a combination of Procrustes analysis and thin-plate splines, the two most powerful tools of landmark-based morphometrics, for multivariate analysis of curving outlines in samples of biomedical images. The thin-plate spline is used to assign point-to-point correspondences, called semi-landmarks, between curves of similar but variable shape, while the standard algorithm for Procrustes shape averages and shape coordinates is altered to accord with the ways in which semi-landmarks formally differ from more traditional landmark loci. Subsequent multivariate statistics and visualization proceed mainly as in the landmark-based methods. The combination provides a range of complementary filters, from high pass to low pass, for effects on outline shape in grouped studies. The low-pass version is based on the spectrum of the spline, the high pass, on a familiar special case of Procrustes analysis. This hybrid method is demonstrated in a comparison of the shape of the corpus callosum from mid-sagittal sections of MRI of 25 human brains, 12 normal and 13 with schizophrenia.
Article
The Argentinean apple snail Pomacea canaliculata is a freshwater gastropod with a high interpopulation variation in shell shape, size and thickness. Previous experimental studies have shown that many life-history traits are highly dependent on rearing conditions. Three natural populations located in one same drainage basin and climatic regime showed marked differences in birth, maturity and maximum sizes. Most of this variation disappeared when newborns from each population were reared under homogeneous conditions in the laboratory, indicating its ecophenotypic origin. However, a significant variation in reproductive, growth and survival patterns attributable to genetic differences among the source populations was still discernible among laboratory cohorts. The three sites studied represent a marked gradient in stability and food availability. Females from the most unstable and poorer site showed a faster prematurity growth and a higher oviposition rate than those from the most stable and productive site. This higher oviposition rate was associated with bigger clutches and a higher mortality rate. The different patterns of survival and somatic and reproductive allocation in the three populations, being heritable and adaptively correlated to different environmental conditions, could be considered as parts of different life-history strategies. Since the 1980s, P. canaliculata has become a serious pest of paddy fields in most Southeast Asian countries. Nearby and recently isolated populations of P. canaliculata from the same basin showed genetically different life-history strategies, so that different populations of this pest could require different control programs.
Article
The shape changes associated with increase in size and sexual dimorphism in Pomacea canaliculata are described using bivariate and multivariate statistical analysis. Allometric growth was found in the studied population, the shell becoming relatively more globose and both aperture and operculum becoming rounder as shell height increases. Related to this ontogenetic change in shell shape is a relative increase in body dry weight. Adult snails show sexual dimorphism, males having both aperture and operculum rounder than females. Because juvenile snails do not exhibit these differences in aperture form, shell dimorphism seems to be associated with sexual maturity; that is, it is possibly related to the development of the penial complex. In summer, adult females of any given shell height weigh significantly more than males of equivalent size; this being possibly due to the remarkable development of the albumen gland in this period. Shell dry weight shows great variability in similarly sized snails, this fact being partially ascribable to the seasonal growth pattern of P. canaliculata in waters showing thermal seasonality.
Article
Despite its widely recognized conchological variation, studies on the shell variability of Pomacea canaliculata are limited to its sexual and ontogenetic components. Here, we analyse the interpopulation variation in conchological and somatic traits, and sex-related growth patterns of P. canaliculata to discover if it is ecophenotypically or genetically determined. Pomacea canaliculata showed variation in shell shape, shell and body weight, and body ash content among populations from three environmentally different sites. Shell shape was also different when snails from the three sources were reared under homogeneous laboratory conditions, indicating a genetic basis for the differences. Shell shapes of laboratory snails differed from, their field counterparts, suggesting an environmental influence on shape. The genetic differentiation of shell shape among the studied populations does not seem to be the outcome of adaptation to local conditions or of genetic drift, but is probably a side effect of adaptive differentiation in some life-history traits. On the other hand, weight and ash content differences disappeared under homogeneous conditions, suggesting that their variation is mainly ecophenotypic. Variability in shell thickness, body weight and ash content seems to be more related to trophic availability than to water chemistry. In the laboratory, females showed slightly higher growth rates than males, but these inter-sex differences varied among snails from the three sources. However, shell length was not different between sexes in the field populations, probably due to a greater effect of food shortage on female growth rates. The widespread pattern that shells of freshwater snails from contrasting environments are different has been attributed mostly to cumulative environmental effects or to adaptation to local conditions. However, we suggest that different shell shapes could arise as a collateral outcome of genetically different reproductive behaviours and that it would be misleading to study the shell as a trait exposed separately to selective pressures or environmental influences.
Article
Pomacea canaliculata is a freshwater snail native from South America that together with some congeners, has invaded natural wetlands and paddy fields in several continents, especially in Southern Asia. The high variability in shape, color and thickness of Pomacea shells and the sexual dimorphism in many traits blurs the species limits and hampers taxonomic identification. Ecological characterization of habitat productivity based on shells was previously proposed for P. canaliculata but was never methodically explored. Using full siblings of P. canaliculata, we studied the effects of different chronic levels of food availability (from 100 to 20% of daily ingestion rate) on shell shape, somatic indices and sexual dimorphism at maturity. The eight specific morphometric and somatic indices investigated showed different combinations of the effects of food availability and sex: changes related to food availability but independent of sex (relative aperture width), sexual dimorphism independent of food availability (shell globosity and relative aperture expansion) and changes related to food availability and sex, without a noticeable interaction (organic density); a significant interaction that increases the intersexual differences when food availability increases was detected in some indices (relative operculum weight, overall shell density and relative shell investment). The organic density could be used as a condition index indicating the actual trophic availability in the field, although it must be estimated separately for males and females. The relative aperture width and the overall shell density could be used as paleo-environmental indicators of productivity, as they can be measured on empty shells, although in the latter variation in water alkalinity must be also considered.
Article
Increasingly, data on shape are analysed in combination with molecular genetic or ecological information, so that tools for geometric morphometric analysis are required. Morphometric studies most often use the arrangements of morphological landmarks as the data source and extract shape information from them by Procrustes superimposition. The MorphoJ software combines this approach with a wide range of methods for shape analysis in different biological contexts. The program offers an integrated and user-friendly environment for standard multivariate analyses such as principal components, discriminant analysis and multivariate regression as well as specialized applications including phylogenetics, quantitative genetics and analyses of modularity in shape data. MorphoJ is written in Java and versions for the Windows, Macintosh and Unix/Linux platforms are freely available from http://www.flywings.org.uk/MorphoJ_page.htm.
Article
Aim To determine the genetic diversity of invasive snails ( Pomacea spp.) that are implicated in crop damage, environmental degradation and human disease, and to determine their distribution pattern in a large part of eastern Asia. Location People's Republic of China (P.R. China). Methods We collected Pomacea snails in a national survey using a grid sampling approach. Overall, 544 snails from 54 sites were used for the present investigation. The mitochondrial cox1 gene was amplified and sequenced from all the snails. We determined and classified the haplotypes using network analyses and mapped them within P.R. China. Haplotypes from this study, together with sequences available from GenBank, were used to reveal the global distribution of Pomacea canaliculata and P. insularum . Results We obtained 521 cox1 sequences and identified 24 unique haplotypes. Six haplotypes were commonly found in P.R. China. Two species, P. canaliculata and P. insularum , and one cryptic group were observed. The distribution of the 24 haplotypes across P.R. China shows a mosaic pattern. Globally, only six of 112 haplotypes of P. canaliculata , P. insularum , P. dolioides , P. lineata and P. paludosa are shared between introduced and native snail populations. We found 16 haplotype clusters, five of which occur in mainland P.R. China. Three of the five clusters could be traced back to South America. The remaining two clusters were unique to P.R. China. Main conclusions Phylogenetic analyses indicate that P. canaliculata , P. insularum and two cryptic groups, discovered by the present and previous studies, coexist in the mainland of P.R. China. The mosaic distribution and the high diversity found in the collection sites suggests multiple and secondary introductions. The findings indicate the importance of preventing further intentional introductions and call for appraisal of the risk posed by these snails in vulnerable areas. Discrimination of the ecological impacts of the different species or genotypes will help to develop setting‐specific management strategies.
Article
Morphometrics is the statistical study of biological shape and shape change. Its richest data are landmarks, points, such as the bridge of the nose, that have biological names as well as geometric locations. This book is the first systematic survey of morphometric methods for landmark data.
Article
Pomacea canaliculata, an apple snail native to South America, has become a serious pest of aquatic crops and a promoter of ecosystem changes in natural wetlands worldwide. Its success as an invader has been attributed to its great phenotypic plasticity in life-history traits. Our aims were to determine the reaction norms of size and age at maturity under a gradient of food deprivation. Full sibling experimental snails were reared in isolation from hatching and maintained until maturity under seven different levels of relative food deprivation based on size-specific ingestion rates. To detect the onset of sexual activity of experimental snails, fully mature virgin snails reared in the laboratory were used as consorts. The reaction norms for age and size at maturity of P. canaliculata showed marked sexual dimorphism. Shell length was the main component of variation in the male reaction norms for both copulation and egg-laying by female consorts, whereas age was the main component of variation for females. Irrespective of the intensity of food deprivation, males mature at the same age at the expense of size, since size is apparently irrelevant in the access to females and male fitness can be maximized through fast maturation. In contrast, a minimum size is required for females to reach maturity, perhaps as a result of their higher reproductive costs. The highly dimorphic reaction norms lead to an increasing lag between male and female maturity as deprivation increases; in temperate regions, males born early in the reproductive season would mature in the same season irrespective of food availability, while most females would have to overwinter before attaining sexual maturity in unproductive habitats or those dominated by unpalatable macrophytes. The great life-history plasticity reported in invaded areas could be a heritage from populations in the native range.
Article
Pomacea canaliculata is the only freshwater snail listed as one of the 100 worst invaders worldwide. Recent studies have demonstrated that small Pomacea snails have higher foraging and competitive abilities than larger snails and hence that ecological and agricultural damage of this invasive snail may be size-dependent. Furthermore, females of P. canaliculata usually reach larger sizes than males, a pattern that results from higher growth rates and not from higher survivorship in females; however, the proximal causes of the sexual dimorphic growth rates are unknown. In this study, we investigate the ingestion rates and growth efficiencies of P. canaliculata in order to explain the ontogenetic and sexual differences in growth and food consumption patterns. Two experiments were performed to study specific ingestion rates and the efficiency in food conversion to body mass at different feeding conditions. Ontogenetic and sexual differences were found in the specific ingestion rates. These decreased inversely with shell length and were higher for females than for males of comparable size. Conversion efficiencies decreased with age in both sexes, in males noticeably earlier than in females. Under high food availability conditions, the decrease is sharper than under low food availability. However, the effect of food availability almost disappeared when in the effect of size was removed. The sexual dimorphism of growth efficiencies and ingestion rates explain why females tend to reach a larger adult size than males, a pattern probably explained by development of the testicle and correlated reduction of mid-gut gland size. Our results on ontogenetic patterns of ingestion rates support predictions that during the reproductive season small snails may cause a great part of the damage to aquatic crops and natural wetlands.
Article
Tributyltin (TBT) has been widely used as antifouling in marine environments, producing imposex in gastropod females (i.e. neoformation of a vas deferens and/or a penis) and shell malformations in bivalves. However, effects of TBT and other pollutants from high marine traffic zones on the shell of gastropods have been little explored. Shell shape in volutids Odontocymbiola magellanica from a harbor polluted site (P) has been compared with that of animals from a non-polluted location (NP) using 3D geometric morphometrics. Also, the microstructure and density of shells from both populations were analyzed. Prior studies made in the same area (Golfo Nuevo, Patagonia, Argentina) based on traditional multivariate morphometricsshowedsomedifferences in size butwasunable to detect differences in shell shapeamong O. magellanica from P and NP areas. Departing from 3D geometric morphometrics, scanning electron microscopy (SEM) and computed tomography (CT) techniques, we have registered the presence of patent differences on shell shape and structure in animals from polluted (P) and non-polluted (NP) areas. In 100% of shells from the NP area we register three calcium carbonate layers (prismatic, cross lamellar and amorphous) and higher densities, while in 50% of the shells collected at the P area the external layer (amorphous) was lacking. Furthermore, a body weight loss of around 30% and a shell weight loss of 20% were registered in animals from the P area. Our combined results suggest that the coordinated use of 3D geometrics morphometrics, CT scan and SEM could be of great utility in order to detect the effect of environmental variables on Neogastropods shell shape and structure.
Article
This account is the result of investigations on living and preserved specimens of Pomacea canaliculata as well as preserved specimens of Pila globosa, Turbinicola saxea and Lanistes ovum bangweolicus. Pilids are amphibious prosobranchs with both a lung and a ctenidium in the mantle cavity. The mantle cavity is broad and shallow, and in addition to the normal pallial complex in these there is a highly extensible pallial inhalant siphon on the left of the head, allowing ventilation of the lung under water, and a fold bordering a longitudinal groove to the right of the head, similar to that in viviparids which creates a separate exhalant channel leading to a samll exhalant siphon. the ctenidium is displaced by the lung to the right and its small leaflets are curved so that they overhang the pallial groove. The hypobranchial gland to the right of the ctenidium extends over the wall of the rectum and genital duct along the right side of the groove. Blood is carried to the lung by the extension of the afferent ctenidial vein and drained from it by the efferent ctenidial vein. In Pomacea an additional afferent vein to the floor of the lung is apparently developed by the horizontal division of the efferent ctenidial vein. To maintain an ample supply of blood at high pressure to the respiratory organs the visceral vein leads directly on to the mantle skirt and has lost its connection with the afferent renal vein. This results in a highly vascular mantle skirt so that a large volume of blood would be forced into the heart on retraction of the snail into its shell; to accommodate this a highly extensible ampulla is developed on the anterior aorta within the pericardial cavity. The kidney, like that of other freshwater prosobranchs, is complex and contains an accessory chamber, overlying the posterior part of the mantle cavity, and which appears to be mesodermal in origin. It is much folded and highly vascular, and is supplied by the afferent renal vein and the renal nerve. The epithelium of the chamber excretes some purines other than uric acid as very fine spherules, whereas in the posterior part of the kidney, large concretions containing uric acid are built up. Blood from the anterior chamber drains into the afferent ctenidial vein; the efferent vessel of the posterior chamber is the homologue of the efferent nephridial vein, although the nephridial gland itself is vestigial. The efferent renal vein to the mantle skirt, which is present in other prosobranchs, has lost its connection with the visceral part of the kidney in pilids.
Article
Apple snails (Ampullariidae: Pomacea) native to the New World have become agricultural and environmental pests widely in southern and eastern Asia since their introduction in about 1980. Although their impacts have been extensively documented, considerable confusion persists regarding their identities and geographical origins. Efforts to resolve the confusion have suffered from inadequate taxonomic and geographical sampling from both native and introduced ranges. Using phylogenetic and genealogical methods, we analysed 610–655 bp of cytochrome c oxidase subunit I DNA sequences from 783 apple snails from 164 Asian locations and 57 native South American locations. In Asia, we found four species of Pomacea in two clades: (1) Pomacea canaliculata and P. insularum, and (2) P. scalaris and P. diffusa. Parsimony networks and mismatch distributions indicate that the non-native ranges of the two most widespread species, P. canaliculata and P. insularum, probably result from multiple introductions. Molecular analyses are consistent with early accounts; non-native P. canaliculata populations trace back to multiple locations in Argentina and have probably been introduced more than once. In contrast, P. insularum was probably introduced from Brazil and Argentina independently. Multiple introductions may, in part, explain the success and rapid spread of these two species. Unlike P. canaliculata and P. insularum, P. scalaris and P. diffusa were probably introduced through the aquarium trade, derived originally from Argentina and Brazil, respectively. Possible physiological, ecological, and native range differences among these four species highlight the importance of accurate identification in understanding invasion patterns and processes, which is vital in developing and implementing management strategies.
Article
... 942 The American Naturalist March-April 1971 GEOMETRIC SIMILARITY IN ALLOMETRIC GROWTH: A CONTRIBUTION TO THE PROBLEM OP SCALING IN THE EVOLUTION OF SIZE Stephen Jay Gould Museum of Comparative Zoology, Harvard University, Cambridge ...
Article
The relationship between ontogenetic, static, and evolutionary levels of allometry is investigated. Extrapolation from relative size relationships in adults to relative growth in ontogeny depends on the variability of slopes and intercepts of ontogenetic vectors relative to variability in length of the vector. If variability in slopes and intercepts is low relative to variability in length, ontogenetic and static allometries will be similar. The similarity of ontogenetic and static allometries was tested by comparing the first principal component, or size vector, for correlations among 48 cranial traits in a cross-sectional ontogenetic sample of rhesus macaques from Cayo Santiago with a static sample from which all age- and sex-related variation had been removed. The vector correlation between the components is high but significantly less than one while two of three allometric patterns apparent in the ontogenetic component are not discernable in the static component. This indicates that there are important differences in size and shape relationships among adults and within ontogenies. Extrapolation from intra- or interspecific phenotypic allometry to evolutionary allometry is shown to depend on the similarity of genetic and phenotypic allometry patterns. Similarity of patterns was tested by comparing the first principal components of the phenotypic, genetic, and environmental correlation matrices calculated using standard quantitative genetic methods. The patterns of phenotypic, genetic, and environmental allometry are dissimilar; only the environmental allometries show ontogenetic allometric patterns. This indicates that phenotypic allometry may not be an accurate guide to patterns of evolutionary change in size and shape.
Article
Morphometrics, a new branch of statistics, combines tools from geometry, computer graphics and biometrics in techniques for the multivariate analysis of biological shape variation. Although medical image analysts typically prefer to represent scenes by way of curving outlines or surfaces, the most recent developments in this associated statistical methodology have emphasized the domain of landmark data: size and shape of configurations of discrete, named points in two or three dimensions. This paper introduces a combination of Procrustes analysis and thin-plate splines, the two most powerful tools of landmark-based morphometrics, for multivariate analysis of curving outlines in samples of biomedical images. The thin-plate spline is used to assign point-to-point correspondences, called semi-landmarks, between curves of similar but variable shape, while the standard algorithm for Procrustes shape averages and shape coordinates is altered to accord with the ways in which semi-landmarks formally differ from more traditional landmark loci. Subsequent multivariate statistics and visualization proceed mainly as in the landmark-based methods. The combination provides a range of complementary filters, from high pass to low pass, for effects on outline shape in grouped studies. The low-pass version is based on the spectrum of the spline, the high pass, on a familiar special case of Procrustes analysis. This hybrid method is demonstrated in a comparison of the shape of the corpus callosum from mid-sagittal sections of MRI of 25 human brains, 12 normal and 13 with schizophrenia.
Article
Pomacea canaliculata is a freshwater snail belonging to the family Ampullariidae, a taxon that includes Asian, African and American species collectively known as apple snails, and is the most widely studied snail in Argentina, being the object of different morphological, anatomical, ecological, embryological and taxonomical studies. Although early recognized, the wide conchological variation of P. canaliculata has been seldom quantitatively analyzed. The aims of our study are to describe and analyze the variation and the origin of P. canaliculata shell traits, and to compare them with the information available for other Neotropical Ampullariids, focusing mainly on quantitative or experimental studies. The shell of P. canaliculata has been described as globose to subglobose, with a low spire and an oval aperture; the color of the shell is brown-green, showing several dark spiral bands of variable width and transverse growth; the operculum is corneous with concentric growth lines around an excentric nucleus. Most of these traits, and many others, show a great influence of ontogenetic, sexual, genetic and ecophenotypic components, which give place to an important intra- and interpopulation variation. In spite of the fact that many aspects of the conchological variation have been already studied, the available information includes, in most cases, only one or a few populations from a restricted geographical region. The knowledge is even more limited for other species of Pomacea or other genera of apple snails, preventing the development of a comparative approach in conchological aspects at generic and familiar levels. The great conchological variation in P. canaliculata has been considered a serious hindrance to the study of several aspects of its biology. However, this apparently chaotic variation can be split in several biologically meaningful components, becoming an interesting subject of research on its own merit.
Sexual dimorphism in Pomacea canalic-ulata. The Veliger 33
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