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A Sticky Thicket of Glue Cells: a Comparative Morphometric Analysis of Colloblasts in 20 Species of Comb Jelly (Phylum Ctenophora)

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A Sticky Thicket of Glue Cells: a Comparative Morphometric Analysis of Colloblasts in 20 Species of Comb Jelly (Phylum Ctenophora) Ciencias Marinas (2020), 46(4):211–225 https://doi.org/10.7773/cm.v46i4.3118 A sticky thicket of glue cells: A comparative morphometric analysis of colloblasts in 20 species of comb jelly (phylum Ctenophora) Una maraña pegajosa de células adhesivas: Análisis comparativo de la morfometría de coloblastos en 20 especies de nuez de mar (filo Ctenophora) Nicholas D Leonardi1, Erik V Thuesen1*, Steven HD Haddock2 1 The Evergreen State College, 2700 Evergreen Pkwy NW, Olympia, Washington, 98505, United States 2 Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, California, 95039, Online ISSN: 2395-9053; Print 0185-3880 United States * Corresponding author. E-mail: [email protected] Abstract. Ctenophores in the class Tentaculata are distinct from Cnidarians in that they use sticky, not stinging, tentacles to capture and subdue their prey. The structures that make these tentacles sticky are colloblasts, specialized multicellular adhesive structures for predation. Located on the tentacles, tentacle side-branches (tentilla), or oral tentilla, colloblasts are only found in comb jellies (phylum Ctenophora). To perform comparative anatomy of the diversity of ctenophore colloblasts, specimens were collected from the epi- to bathypelagic zones near the coasts of central California and the Hawaiian Islands using blue-water divers and remotely operated vehicles. Tentacle samples were immedi- ately fixed in a 4% formalin solution at sea, and then prepared in the lab via secondary fixation in 2% OsO4 for scanning electron microscopy (SEM). Diversity of ultrastructural characteristics was observed using SEM, and the morphometrics of the collosphere, external secretion granules, and spiral filament were recorded for 20 species, within 9 families and 9 genera, including 13 undescribed species. Morphometry of colloblasts reveals that the shape of the collosphere (the organizational unit of sticky granules) falls into 3 classifications: spherical, ellipsoidal, or non-uniform. External secretion granule deposition falls into 2 categories: clustered or patterned; the cap cell membrane was either present or absent. This morphological variation is summarized graphically and will be useful to describe the functional diversity and feeding ecology of the interesting and controversial phylum Ctenophora. Key words: colloblast, ctenophore, predation, scanning electron microscopy, Tentaculata. Resumen. Los ctenóforos de la clase Tentaculata difieren de los cnidarios en que usan tentáculos pegajosos y no punzantes para capturar y dominar a su presa. Las estructuras que vuelven a los tentáculos pegajosos son los coloblastos, estructuras pluricelulares adhesivas especiali- zadas para la depredación. Localizados en los tentáculos, en las ramificaciones de los tentáculos (tentilas) o en las tentilas orales, los coloblastos solo se encuentran en las nueces del mar (filo Ctenophora). Con el fin de realizar una comparación anatómica de los distintos coloblastos en ctenóforos, se recolectaron especímenes desde la zona epipelágica hasta la batipelágica cerca de la costa central de California y de las islas hawaianas utilizando buceo científico (blue-water diving) y vehículos sumergidos operados remotamente. Las muestras de tentáculos fueron inmediatamente fijados en el mar en una solución de formalina al 4%, y luego fueron preparados en el laboratorio vía una solución secundaria de OsO4 al 2% para microscopía electrónica de barrido (MEB). La diversidad de características ultraestructurales fueron observadas utilizando el MEB, y la morfometría de la coloesfera, los gránulos externos de secreción y los filamentos espiralados de 20 especies fueron registrados, dentro de 9 familias y 9 géneros, incluidas 13 especies no descritas. La morfometría de los coloblastos revela que la forma de la coloesfera (la unidad organizacional de gránulos pegajosos) presenta 3 clasificaciones: esférica, elipsoide o no uniforme. La disposición de los gránulos externos de secreción presenta 2 categorías: en cúmulo o en patrón; la membrana de células externas estaba presente o ausente. Esta varia- ción morfológica está resumida en gráficos y será de utilidad para describir la diversidad funcional de este interesante y controversial filo Ctenophora. Palabras clave: coloblastos, ctenóforos, depredación, microscopio electrónico de barrido, Tentaculata. Introduction Introducción Ctenophora is a diverse phylum of gelata consisting of Ctenophora es un filo variado de zooplancton gelatinoso about 190 described species, with estimates for the number que consiste de casi 190 especies descritas, y se estima un of additional undescribed species being roughly equiva- número adicional de especies no descritas casi equivalente lent (Appeltans et al. 2012). Molecular and phylogenomic (Appeltans et al. 2012). Los análisis moleculares y filoge- analyses of ctenophores have indicated that they may be the nómicos de los ctenóforos han indicado que podrían llegar sister group to all other animals (Dunn et al. 2008, Whelan a ser un grupo hermano de todos los animales (Dunn et al. et al. 2017, but see Simion et al. 2017). Dunn et al. (2015) 2008, Whelan et al. 2017, pero ver Simion et al. 2017). Dunn Screened via Similarity Check powered by iThenticate 211 Open Access Ciencias Marinas, Vol. 46, No. 4, 2020 highlighted that nonbilaterian phyla do not only possess et al. (2015) han subrayado que los filos no bilaterales no simple traits but also complex and unique traits, as do bilate- solamente poseen rasgos simples, sino también rasgos únicos rians, making it important to describe traits across all animal y complejos como los bilaterales, lo cual resalta la impor- phyla in order to properly compare evolutionary relation- tancia de describir los rasgos en todos los filos animales para ships and diversification. poder comparar adecuadamente las relaciones evolutivas y Ctenophores are the only organisms that possess collo- la diversificación. blasts, specialized adhesive structures for predation. The Los ctenóforos son los únicos organismos que poseen colo- diversification of feeding behaviors in ctenophores is in part blastos, estructuras adhesivas especializadas para la depreda- due to the presence or absence of tentacles containing col- ción. La diversificación en el comportamiento alimentario loblasts, and the manner in which they are arranged (Komai en los ctenóforos se da, en parte, gracias a la presencia o 1922, Mackie et al. 1988, Emson and Whitfield 1991, ausencia de tentáculos que contienen coloblastos y la manera Matsumoto and Harbison 1993, Haddock 2007). Through en la cual éstos se encuentran ordenados (Komai 1922, the use of electron microscopy, morphometrics of colloblasts Mackie et al. 1988, Emson y Whitfield 1991, Matsumoto y have been recorded for some species (Bargmann et al. 1972; Harbison 1993, Haddock 2007). Mediante el uso de micros- Benwitz 1978; Franc 1978; Mackie et al. 1988; Emson and copía electrónica, la morfometría del coloblasto ha sido regis- Whitfield 1991; Carré and Carré 1993a, b; Eeckhaut et al. trada para algunas especies (Bargmann et al. 1972; Benwitz 1997), but only one study has compared variation in collo- 1978; Franc 1978; Mackie et al. 1988; Emson y Whitfield blasts across a small portion (4 species from 4 families) of 1991; Carré y Carré 1993a, b; Eeckhaut et al. 1997), pero the phylum (Franc 1978). Colloblast polymorphisms within a solo un estudio ha comparado la variación de coloblastos en species have only been observed in Minictena luteola (Carré una pequeña porción (4 especies de 4 familias) del filo (Franc and Carré 1993b). The vocabulary associated with collo- 1978). El polimorfismo de coloblastos dentro de una especie blasts has long been confused, but von Byern et al. (2010) ha sido observado únicamente en Minictena luteola (Carré y have recently clarified a standard terminology, which is used Carré 1993b). El vocabulario asociado con los coloblastos ha herein (Fig. 1). The goal of the present study is to survey sido confuso por mucho tiempo, pero von Byern et al. (2010) the diversity of colloblast characteristics across the phylum recientemente aclararon una terminología estándar, que es through the use of scanning electron microscopy (SEM) and la que se utiliza en este documento (Fig. 1). El objetivo del morphometric analyses. presente estudio es examinar la diversidad de las caracterís- ticas de los coloblastos en el filo mediante el uso de micros- Materials and methods copía electrónica de barrido (MEB) y análisis morfométricos. Twenty species of ctenophores were collected from Materiales y métodos the epi- to bathypelagic zones off the coasts of central California and the Hawaiian Islands. These locations are Veinte especies de ctenóforos fueron recolectados desde la advantageous because of their relatively near-shore access zona epipelágica hasta la batipelágica, cerca de la costa central to very deep environments (Haddock et al. 2017). Shallow de California y de las islas hawaianas. Estos sitios son venta- species were hand-collected in glass jars by blue-water josas por presentar ambientes muy profundos a una relativa divers (Haddock and Heine 2005). Meso- and bathypelagic cercanía de la costa (Haddock et al. 2017). Especies de aguas species were collected using suction samplers and detritus someras fueron recolectadas a mano en frascos de vidrio por samplers on remotely operated vehicles from the Monterey buzos científicos (Haddock y Heine 2005). Especies de las Bay Aquarium Research Institute (Robison 1993). When zonas meso
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