Exploring intraspecific morphological variations in Parvocalanus crassirostris (F. Dahl, 1894) (Copepoda: Paracalanidae) in the Gulf of Oman

doi:10.21203/rs.3.rs-5256461/v1

In this study, morphological characters instability in adult females of Parvocalanus crassirostris (F. Dahl, 1894) is evaluated. This species shows differences in shape, segmentation, spine size, and presence or absence of spines on 5th legs and serration of outer edge of exopod 2 and 3 in legs 2–4. Accordingly, in female individuals of P. crassirostris more than 28 and five types were observed in P5 and ornamentation of P2–4, respectively. In this study, all observed morphs are described to provide informative data for evaluating diverse characters types. These variations seem to be density-dependent. Among state-of-the-art methods, the confocal laser scanning microscope was used to examine this unresolved phenotypic diversity and refer to the main patterns and hypotheses related to the factors affecting morphological traits inconsistencies in this species.

discriminative characters

morphological variations

character validity

phenotypic diversity

Planktonic copepods are key elements in marine environments. Among these, calanoids are important because of their highest diversity and abundance (Stephen 1984; Melo et al. 2014). Moreover, they play a central role as energy transporters in marine food webs, bioindicator for assessing the pollution in the marine environments, medicine, and pathogenicity and also in biological control (Benz 2005; Melo et al. 2014; Anufriieva 2015; Abo-Taleb et al. 2020). Previously, most of the studies on calanoid copepods in Chabahar Bay, Gulf of Oman have been devoted to ecological aspects and environmental pollution, but taxonomic studies were infrequent and recently began. Therefore, it was essential to conduct a study on the identification and diversity of calanoid species in this area. The Chabahar Bay is ecologically rich due to its ecosystem and species diversity. The area is currently considered for economic investments because of direct access to the Indian Ocean, and accordingly encountered human activities and their impacts. This is now considered as one of the sensitive marine areas and subject to few scientific studies (Fazeli et al. 2010; Fazeli et al. 2015). During ongoing study on taxonomy of calanoid copepods in the Chabahar Bay, some morphological variations were observed in characters of Parvocalanus crassirostris (F. Dahl, 1894) These include extensive differences in shape, leg segments, size of spine-like setae, and presence or absence of spines on the 5th legs. In addition, there are five types of ornamentations on the outer margins of exopod segment (Exp) 2–3 in legs 2 to 4 (P2–P4) in P. crassirostris. According to Vidjak et al (2016) the new genus Parvocalanus was designated by Andronov (1970), which included several small species previously classified as Paracalanus Boeck, 1865, based on the shape of the rostrum, structure of fifth leg female and the appearance of male cephalon. At first, F. Dahl (1894) provided a short description of this female specimen from an estuary on the Atlantic coast of Brazil. Thereafter, some of the variations in this species have been documented; Davis (1944) described the material from Chesapeake Bay as P. crassirostris var. nudus in which there are four types of serrations on the outer edge of the 3rd segment of the exopod. Wellershaus (1969) described this species as P. crassirostris cochinensis nova forma in the Cochin Backwater and expressed that this form “cochinensis” is not wholly uniform in the spinulation of the outer margins of the exopods of the female legs. These variations were seen as Exp 2 in P2 without spines, P3–P4 proximal and distal part of exopodal segment 2 with spines and Exp 3 of P2–P4 proximal and distal part with spines and armature on swimming legs which are different from “sewelli” form. Then, Greenwood (1976) described P. crassirostris forma typica (as P. crassirostris typica Früchtl, 1924) with some recorded variations in the number of spines on proximal outer margins of exopodal segment 3. Finally, all the names of the morphotypes of this species have been synonymized and it was designated under the name P. crassirostris (F. Dahl, 1894). In the present study, these morphological variations caused taxonomic ambiguities in identification of material from Gulf of Oman. The main goals of this study were (i) to find the taxonomic value of variable 5th legs using state of the art microscopic techniques and (ii) to discuss the possible factors causing morphological variations in 5th legs.

Adult specimens were collected from five stations in the Chabahar Bay during four successive seasons (Table 1). Samplings were conducted using 100 µm Hydrobios® plankton net towed horizontally on the sea surface for 10–15 minutes at midnight to down. Then, specimens were immediately fixed in 96% ethanol for long-term preservation and transferred to the laboratory of Animal Biosystematics, University of Tehran and were used for taxonomic identification. Material of P. crassirostris was deposited at the Zoological Museum, University of Tehran (ZUTC 7084). First, the material was sorted under a stereomicroscope and then, adult specimens of P. crassirostris were selected for this survey. Morphologically, the female individuals of P. crassirostris presented great variations in the numbers and shape of the segments, spine size, presence/absence of spines on the 5th legs. This species with differed legs was compared with the normal individuals of P. crassirostris which were described by Vidjak et al (2016) and here in this study considered as “normal type”. The morphological examination of these individuals was carried out under a light microscope and then, specimens were placed in a drop of glycerin in lateral view and then dissected with two sharp needles, one needle was used in holding the specimen and the other to dissect the appendages under a stereomicroscope. Before dissection, whole animal body was stained with a dye that contains a ratio of one to one from Congo red and Fuchsine and then mounted on slides with a drop of glycerin and coverslips sealed with nail varnish. The whole body and dissected parts were photographed using light and Confocal Laser Scanning Microscopes. Moreover, drawings were made in detail with a Camera Lucida fitted on compound microscope and digital inking were prepared with Adobe Illustrator and Adobe Photoshop. The pattern of armature formula of swimming legs (P₁–P₄) is adopted from Huys and Boxshall (1991). To determine frequency of occurrences of the variations in the population of P. crassirostris, the Cross-Tabulation Analysis and Chi-Square were used to assess significant differences between normal and individuals with variable morphs among seasons. In this study, among the five stations (Table 1), the female specimens from two stations (Shahid Beheshti and Shahid Kalantari) were considered seasonally.

Table 1

Coordinates of sampling sites in Chabahar Bay
Seasons 2021–2022	Stations	Coordinates
Pre-monsoon	Shahid Beheshti port	25˚17΄ 50˝N 60˚36΄42.32˝E
Winter monsoon	Shahid Kalantari port	25˚18΄37˝N 60˚37΄37.29˝E
Post-monsoon	Tiss fishing port	25˚21΄18˝N 60˚35΄59.52˝E
Summer monsoon	Vicinity of Haft-e-Tir River mouth	25˚17΄47˝N 60˚37΄32.31˝E
	Center of Chabahar Bay	25˚20΄55˝N 60˚30΄44.76˝E

Morphological variations in Parvocalanus crassirostris

Body: length 0.52 – 0.65 mm, small and stout, tapering towards the forehead uniformly. Prosome 5-segmented; Cephalosome incorporating first pedigerous somite; 4^th and 5^th pedigerous somites completely separated (Fig. 1). Rostral filaments bifurcated, short and blunt. Cephalic dorsal hump prominent in lateral view. Antennule (Fig. 4a): 25-segmented, extending to as far as anal somite. Posterolateral corners of pedigerous somite rounded, prosome length about three times as long as length of urosome plus caudal rami, urosome 4-segmented consisting of genital double-somite, two free somites and anal somite (Fig. 6f); genital double-somite symmetrical, swollen anterolaterally, broad, rounded dorsally, genital somite wider than urosome somites 2 and 3, genital system symmetrical with paired gonopores on the sides (Fig. 7), anal somite longer than second and third urosomal somites. Caudal rami symmetrical, each with four caudal setae.

Antenna (Fig. 5a): biramous; basis with two setae; endopod 2-segmented, first segment with 2 setae; second segment bilobate, with proximal and distal lobes bearing eight and six setae, respectively. Exopod 6-segmented, setal formula 3, 1, 1, 1, 1, 4.

Mandible (Fig. 4b, 5c): with a pair of jointed structures called mandibular palp and gnathobase (Fig. 5b). Gnathobase with a ventral tooth and several central and dorsal teeth, and a spine like seta. Mandibular palp biramous, basis with three setae, exopod 6-segmented, setal formula 1, 1, 1, 1, 1, 1; endopod 2-segmented bearing three and 12 setae on proximal and distal segments, respectively.

Maxillule (Fig. 4c, 5d): praecoxal arthrite with 6 setae and 9 spines. Coxa with three setae on endite; epipodite with seven setae. Basis bearing four and five setae on proximal and distal endites, respectively. Exopod with 11 setae. Endopod 3-segmented, first to third segments bearing 3, 5 and 7 setae, respectively.

Maxilla (Fig. 4d, 5e): Praecoxa and coxa with 4 endites bearing 5, 3, 3, 3 setae; basis with 1 endite, bearing 4 setae and one seta in dorsal view. Endopod 3-segmented with setal formula of 2, 2, 3.

Maxilliped (Fig. 4e, 5f): Praecoxa with one seta, coxa bearing seven setae; basis with three setae ventrally and one seta dorsally. Endopod 8-segmented; first to eighth segments bearing 2, 4, 4, 4, 1, 4, 1 and 3 setae, respectively.

Swimming legs with 3-segmented exopods; endopod 2-segmented in P1, 3-segmented in P2–4 (Fig. 6a–d). Proximal outer edge serrated in Exp3 of P2–P4 with 5, 11 and 10 spinules, respectively. Segments 2–4 bearing 28 types of variations in size, shape and number of segments and the terminal spine like setae (Fig. 2a–y, 3a–b, 6e). P5 with 2–4 segment, asymmetrical. First segment slightly robust. Normal individuals with 2-segmented and symmetrical P5 (Fig. 3c).

The pattern of armature formula on P1–P4 is presented in Table 2. The specimens with morphological variation and normal forms in P5 show some differences in serration of outer margin of Exp 1–3 of P2–4. These variations are classified into the followings five types in which Exp2 outer margin is smooth in all groups (examples of some morphotypes are given in Fig. 8a-e).

Morphotype I, In P2, Exp3 outer proximal and distal margins serrated. In P3–P4, Exp2 outer margin and Exp3 outer proximal and distal margins serrated.

Morphotype II, In P2, Exp3 outer proximal margins serrated, distal margin smooth. In P3–P4, Exp2 outer margin smooth and Exp3 outer proximal margin serrated; Exp3 outer distal margin smooth.

Morphotype III, In P2, Exp3 outer proximal margin serrated, distal margin smooth. In P3, Exp2 outer margin and Exp3 outer proximal and distal margins serrated. In P4, Exp2 outer margin and Exp3 outer proximal margin serrated and Exp3 outer distal margin smooth.

Morphotype IV, Exp3 outer proximal margin serrated, distal margin smooth. In P3–P4, Exp2 outer margin and Exp3 outer proximal and distal margins serrated.

Morphotype V, Exp3 outer proximal margin serrated, distal margin smooth. In P3, Exp2 outer margin and Exp3 outer proximal and distal margins serrated. In P4, Exp2 outer margin smooth and Exp3 outer proximal margin serrated; Exp3 outer distal margin smooth.

It is noteworthy that these serration patterns were observed in individuals from all localities at the Chabahar Bay.

Table 2 Spine and setal formula^* of swimming legs 1–4 in P. crassirostris

Leg	Coxa	Basis	Exopod			Endopod
			1	2	3	1	2	3
1	0-0	0-0	0-1	0-1	II-I-4	0-1	1, 2, 2	_
2	0-1	0-0	I-1	I-1	II-I-5	0-1	0-2	2, 2, 3
3	0-1	0-0	I-1	I-1	II-I-5	0-1	0-2	2, 2, 3
4	0-1	0-0	I-1	I-1	II-I-5	0-1	0-2	2, 2, 3

* In setal formula, roman characters in left represent spine like seta; middle shows apical long seta and left number belong to lateral long seta.

Statistical Analyses of morphological variations

The individuals of P. crassirostris were observed with frequency of 37 and 401 individuals with variable and normal morphs in winter, respectively (Table 3). Significant differences (p< 0.0005) were observed between these two types of individuals with respect to seasons. While considering annual frequency, it was found that among female P. crassirostris, 7.8% presented morphological variability in their fifth legs, whereas 92.2% of these showed normal types.

Table 3 The seasonal abundance of individuals with variable and normal morphs in P. crassirostris at each station

Stations	Pre-monsoon 2021		Winter monsoon 2022		Post-monsoon 2022		Summer monsoon 2022
Stations	1	2	1	2	1	2	1	2	Total
variable morph	7	4	19	18	3	9	4	7	71
normal morph	59	18	213	188	161	71	33	98	841

The largest number of occurrences of deformed specimens was recorded in winter monsoon and the lowest morphological variation values was observed in P. crassirostris in Pre-monsoon (Fig. 9).

Specifically, the morphological variations in crustaceans have been subject to extensive research due to their relevance in understanding evolutionary processes and ecological interactions (e.g., Palmer 2005, 2016; Duffy 2007; Melo et al. 2014; Souissi and Souissi 2020; Olesen and Grygier 2024). Historically, remarkable focus has been devoted to morphological variation in the research on copepods taxonomy and evolution (Lajus and Alekseev 2000). Different authors proposed some evidences to clarify these intraspecific variations. These variations are caused by genetic and non-genetic factors, and the latter includes the following examples:

Density dependent changes: the effects of higher frequency of individuals in a population are sometimes reflected in the form of morphological changes, especially when density leads to food shortages (Mayr and Ashlock 1991).
Food density and quality: the effect of food availability or limitation is known as another determinant factor that was considered as one of the causes for observed appendages abnormalities (see Tonolli, 1971; Villalobos and Zuniga, 1991). Additionally, according to Mauchline )1998(, both the quantity and quality of food are well-established factors affecting reproduction and development in copepods.
Physical and chemical environmental effects: Villalobos and Zuniga (1991) referred to the key parameters of the lakes, such as the temperature, salinity, and oxygen concentration. These are most likely the main factors influencing the variability of the body size and appendages in the invertebrate communities.
Predator effects: The differential presence of predators may be leading to morphological variability (see Villalobos and Zuniga, 1991) depending on the kind of predators such as fish or invertebrates.
Mid-ultraviolet effects: negative effects of mid-ultraviolet radiation specifically UVB from 280 to 320 nm have appeared to cause deformations in planktonic copepod (Naganuma et al. 1997; Kouwenberg et al. 1999; Lacuna and Uye 2000; Lee et al. 2014).
Bacterial or viral infections and chemicals agents: These may be the causes of teratogenic deviations (Brent and Beckman 1990). Whether morphological deformities are induced by environmental factors or not, these structures must have either a genetic or teratogenic origin (see Pandourski and Evtimova 2005).

These factors cause a series of phenomena in organisms, including abnormalities and deformities (Weis et al. 1992; Naganuma et al. 1997; Primavera and Quinitio 2000; Jagadeesan and Jyothibabu 2016), intersexuality (Gusmão and McKinnon, 2009) and asymmetry. The asymmetry was subject to many works and across wide range of species (Palmer, 1996a) being addressed from different aspects such as developmental stability, pollution, parasitism and stress indicator (Ostbye et al. 1997; Lajus et al. 2015b; Reimchen, 1997; Leary and Allendorf 1989). In their study, Gusmão and McKinnon (2009) found two main factors influencing the occurrence of intersexes in copepods including resource availability and possibly parasitization which is linked to food deficiency. In addition, they referred to the copepod intersexuality in P. crassirostris, as a common occurrence of characters variability. This phenomenon occurs when a modified 5^th leg appears in the intersex individuals (feminized male) which is resemble to the male leg (see Souissi et al. 2010).

Ludwig (1932) and Palmer et al. (1993) showed that the external shape of the body of most animals is bilaterally symmetrical, deviation from symmetry creates variation in their shape. There are three types of bilateral asymmetry (see Palmer and Strobeck 1986; Rowe et al. 1997) including: Fluctuating Asymmetry (FA), Directional Asymmetry (DA) and Antisymmetry (AS).

The present study illustrates a high degree of intraspecific morphological variations in the 5^th legs in females of P. crassirostris in several localities at the Chabahar Bay. In this study, over 28 morphotypes of P. crassirostris has been found. These characters diversities were found in the shape, size, and number of segments and also presence of spines on the left and right legs. In addition, the other character varieties were noted in different serration patterns on the outer margins of the Exp in P2–4 in P. crassirostris. Accordingly, the morphological variations among morphotypes of P. crassirostris are taxonomically controversial. In addition, the morphological analyses were supported using molecular markers in this species to conclude whether the documented variations represent any genetically differentiated populations. Noticeably, mitochondrial Cytochrome Oxidase subunit I (COI) analysis revealed that all examined material including different and normal morphotype individuals belong to the same species. Therefore, these various characters considered as intraspecific variations. This diagnostic character used by Shih et al (2022), based on observed vaiabilities in 5^th legs, this should be used with caution in identification of P. crassirostris individuals.

It seems that the observed variations in P. crassirostris follows random pattern of character instability due to a high bilateral variety of fifth legs which is repeated on both left and right sides.

In the present study among the mentioned factors causing intraspecific variations in P. crassirostris, these seem to be related to density dependent changes. Since, during this survey, the highest abundance belonged to members of the Paracalanidae compared to other families within Calanoida. In this family, P. crassirostris individuals with normal legs were observed in all sampling localities during four consecutive seasons as one of the most abundant species in the study area at any water temperature. However, population density is probably one of the reasons for morphological variabilities in P. crassirostris, as this enhances morphological diversity in individuals (see Mayr and Ashlock 1991).

The present study indicates a 7.8% annual share of specimens with variable morph in P. crassirostris. Individuals with variable and normal fifth legs in P. crassirostris showed a higher frequency in winter and spring seasons. In general, the percentage of occurrence in normal and variable individuals showed a significant difference in this species.

According to Mauchline (1998), basically calanoid copepods are bilaterally symmetrical but several characters in different species are noticeably asymmetrical (Ferrari and Hayek 1990) such as geniculate antennule and 5^th pair of swimming legs in male, and genital somite in female. Generally, in Paracalanidae, as defined by Moon et al (2014), shape of distal segment and presence of spine on the 5^th leg are the main taxonomic characters at the species level. In a study by Bauer and Martin (1991), the 5^th legs in females are symmetrical but usually reduced or absent.

In this study, the actual functional significances of these morphological variability are unclear. According to Watling and Thiel (2012), the 5^thlegs are sexually dimorphic. The female fifth leg plays a key role in reproduction of some calanoid copepod families (Ohtsuka and Huys 2001) with removing the discharged spermatophores.

Asymmetry has positive and negative effects on reproductive success (e.g., Thornhill 1992; Møller 1993; Harvey and Walsh 1993; Liggett et al. 1993; Swaddle and Cuthill 1994a, 1994b; Thornhill and Gangestad 1994; McLachlan and Cant 1995; Møller and Thornhill 1998). Notably, in most copepods, the fifth swimming leg is used more during reproduction than swimming and specifically in mating process and spermatophore transfer in male and cleaning debris in female (see Marshall and Orr 1972; Watling and Thiel, 2012). Based on Watling and Thiel (2012), longer and wider legs of larger copepods help them move farther in one stroke, while smaller copepods take multiple strokes to move the same distance. Thus, the species with short legs are able to increase their speed and periodic movements, while the species with longer legs encounter resistance swimming, moving continuously in a smooth cruising pattern. But this is not the case in individuals with reduced or modified 5^th legs.

In some copepods, such as the current study species, the fifth legs are reduced. Therefore, the other swimming legs play a role in jumps. In their study, Kiørboe et al. (2010) stated that after the strike of first legs and shortly the others, because of ventrally positioned legs, a rotation occurs after each leg beating along antero-posterior and also around lateral axes. Accordingly, urosome is bent forward step by step to compensate for the rotation effects caused by each leg strikes. It seems, in copepods with four long and active legs such as the species of current study, the reduced 5 legs are used in lesser extent in stabilization, maneuvering and control of movement during jumping cruise helping with balance and orientation maintenance in the water.

Watling and Thiel (2012) argued that each appendage is morphologically adapted to perform a specific function that enhances survival and reproduction. This is, according to West-Eberhard (2003), the ability of organisms to change their body shape and structure in response to environmental changes.

In addition, Svanbäck and Eklöv (2002) mentioned that morphological differences at intra-specific or population levels are persistently addressed as adaptations to various ecological conditions.

It seems that fifth leg in P. crassirostris is bifunctional and helps the organism both in mating and swimming accuracy, and with the variability created in this appendage, it may have a positive or negative effect on the functional quality of breeding biology, signaling, and swimming in these organisms. Morphological variabilities in the left and right legs of P. crassirostris may formed by their functional importance in stressful conditions, possibly the high population density. The biological significance of variability is useful for the evaluation of developmental precision of individuals and populations. It should be used to investigate the impacts of environmental and genetic stresses on the organisms as a biomonitoring toll (see Palmer 1996b) in ecological monitoring and conservation biology. Finding developmental and evolutionary significance of these morphological instability is necessary to understand the adaptation and evolution of species in their complex marine environmental.

The morphological variations in material of P. crassirostris in current study leading to confusion regarding the identification of these species. Consequently, these variable 5^th legs should not be considered as a superior discriminative character for identification of these species or should be used with careful examination of several specimens to find character stability with higher frequency. According to current observations, among the afore-mentioned factors that cause morphological diversity among individuals, the explanations for presence of these deviated morphs may be related to the high population density of P. crassirostris in Chabahar Bay at different sampling location and season. Also, these variabilities in characters could be used as a factor to evaluate individuals condition and developmental instability. This is recommended for further investigations to explore the cause of these morphological variations, as well as their potential impact on the copepod fitness, survival, and interaction with its marine environment. There was no prior study on the morphological instabilities of the legs in P. crassirostris with documented variations, but this is recorded in the current morphological survey. In addition, there are no quantitative or experimental information on character validity or development. Analysis of the individuals in controlled laboratory conditions or mesocosm will possibly allow the recognition of the factors resulting in observed morphs. How these organisms adapt to their environment and survive in natural and anthropogenic conditions are crucial in our understanding of aquatic biodiversity conservation and ecosystem health.

P₁–P₅, first to fifth swimming legs; CLSM, Confocal Laser Scanning Microscope.

Acknowledgements

We are grateful to the Iran National Science Foundation for partial financial support of this work (INSF grant no. 99022227), in particular, to A. S. and R. F. Special thanks also go to the Ministry of Science, Research, and Technology of Iran, and the University of Tehran for supporting R. F. during her visiting period in Germany. We would like to thank Dr. Jasmin Renz-Gehnke for providing the facilities for R. F. at the Senckenberg German Centre for Marine Biodiversity Research, and we extend special thanks to Dr Nancy Mercado-Salas for her generosity in providing high-quality CSLM images at the Leibniz Institute for the Analysis of Biodiversity Change, Zoologisches Museum, Hamburg. The sampling would have been impossible without the help of Mr. A. Rigi-Mirkazehi, whose contribution is acknowledged.

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No competing interests reported.

Exploring intraspecific morphological variations in Parvocalanus crassirostris (F. Dahl, 1894) (Copepoda: Paracalanidae) in the Gulf of Oman

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Version 1

Abstract

Figures

Introduction

Material and methods

Results

Morphological variations in Parvocalanus crassirostris

Discussion

Conclusion

Abbreviations

Declarations

References

Additional Declarations

Status:

Version 1